Journal of Ecology 2002 90, 472479
2002 British Ecological Society
Blackwell Science, LtdResponses of Pancratium sickenbergeri to simulated bulb herbivory: combining defence and tolerance strategies
NATALIA RUIZ*, DAVID WARD* and DAVID SALTZ**Mitrani Department of Desert Ecology, Jacob Blaustein Institute for Desert Research, Ben Gurion University of the Negev, Sede Boqer 84990, Israel, Department of Biology, National University of Colombia, Bogota A.A. 7495, Colombia, and Department of Nature Conservation, University of Stellenbosch, Matieland 7602, South Africa
1 We determined the effects of simulated bulb herbivory by the dorcas gazelle, Gazelladorcas, on the geophyte, Pancratium sickenbergeri (Amaryllidaceae), in the Negevdesert, Israel. In a population with a high level of herbivory, we removed 0%, 25%, 50%and 75% of bulb tissue from plants.2 Bulbs with an intermediate volume removed (50%) showed the highest re-growthcapacity and fitness in relation to the other cutting treatments. The production of cal-cium oxalate defences increased in cut bulbs.3 There was a trade-off between investment in storage and defence. Trade-offs were notfound between growth and defence, between growth and reproduction or betweenreproduction and defence.4 Control plants grew less, had lower levels of calcium oxalate, stored more energy andproduced more flowers and fruits, but their current fitness was only slightly higher thanin the intermediate cutting treatment (50%) because of the high abortion of fruits.5 P. sickenbergeri showed a complex resource allocation pattern as the result of com-bining defence and tolerance of herbivory. Plants respond to high herbivory levels witha high re-growth capacity as a tolerant mechanism to maintain fitness.
Key-words: calcium oxalate, geophytes, plant defences
Journal of Ecology (2002) 90, 472479
Plants can use stored compounds to replace tissue lostby browsing of photosynthetic area and for futuresupport of biosynthesis for growth or other plant func-tions (Chapin et al. 1990; Pugliese & Kozlowski 1990;Marquis et al. 1997). However, investment of limitingresources by a plant in stored reserves diverts thesesame resources from the growth of reproductive andphotosynthetic tissue. Costs and benefits of storage areestimated through the opportunity costs of storage, i.e.the benefit achieved from the most favourable alter-native pattern of allocation. The greater the risk (i.e.where there is a high probability of a large or frequentloss), the more a plant should store resources tosupport future growth and reproduction (Dafni et al.1981; Chapin et al. 1990).
Species adapted to arid environments have inher-ently low growth rates and frequently accumulate largenutrient stores to allow them to respond quickly torainfall (Noy-Meir 1973; Boeken 1990; Chapin et al.1990). Under these conditions, physiological trade-offsare caused by allocation decisions between storage,growth, maintenance, reproduction and defence(Stearns 1992; Zangerl & Bazzaz 1992; Mole 1994).Therefore, selection exerted by herbivores interactswith resource availability to result in fitness trade-offsassociated with different resource allocation patternsin different environments (Herms & Mattson 1992).That is, selection by herbivores may create sufficientenvironmental variability (Ward & Saltz 1994) to affectthe allocation pattern that is adapted as a result of thedamage experienced by the plant.
In geophytes, bulbs serve both as sinks and sources,and change carbohydrate composition as they growand develop (Theron & Jacobs 1996). Before new foli-age provides photosynthates, growth depends onreserves deposited and stored in leaf bases during thepreceding season. Reserves are used for the develop-ment of new leaves (foliage and bases) and roots. Once
Correspondence: David Saltz, Mitrani Department of DesertEcology, Jacob Blaustein Institute for Desert Research, BenGurion University of the Negev, Sede Boqer 84990, Israel (fax972-8-65967771, e-mail email@example.com).
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2002 British Ecological Society, Journal of Ecology, 90, 472479
the foliage becomes the photosynthate source, resourcesare stored in old and new leaf bases. The inflorescencebecomes the major sink when elongation of the flowerstalk is initiated (Theron & Jacobs 1994). Thus, geo-phytes, and especially hysteranthous geophytes (thosein which the inflorescence appears during the leaflessphase), are expected to possess great efficiency and flex-ibility of utilization compounds stored in their bulb(Dafni et al. 1981; Boeken 1990; Ruiters et al. 1993)and therefore plants might change their allocation ofresources according to herbivore pressure.
We studied the effects of simulated herbivory byremoving different amounts of tissue from bulbs on theconsequent growth, reproductive performance anddefence of Pancratium sickenbergeri (C. et Barbey Amaryllidaceae) in a population subject to high levelsof grazing. P. sickenbergeri is a hysteranthous geophytecommonly found in sand dunes of the Negev Desert,Israel. It is characterized by three phenological stagesconsisting, respectively, of inflorescence, leaves and noabove-ground biomass: all stages are subject to herbiv-ory by dorcas gazelles (Gazelle dorcas) (Ward & Saltz1994; Saltz & Ward 2000). When there is no above-ground biomass, the gazelles dig for underground partsof P. sickenbergeri and may consume all or part of thebulb, which contains most of the plants volume (Ward& Saltz 1994). During this time, 5088% of the plantshave their underground parts partially consumed andbetween 5% and 10% are completely consumed (i.e. thebulb is removed). Thus, gazelles are expected to exertstrong selection on the development of antiherbivorestrategies. P. sickenbergeri exhibits a combination ofdefence mechanisms consisting of both tolerance(defined as the capacity of a plant to maintain its fitnessthrough growth and reproduction after sustainingherbivory damage, Rosenthal & Kotanen 1994) andavoidance (Ward & Saltz 1994; Ward et al. 1997; Saltz& Ward 2000). Avoidance strategies include bulbsgrowing deeper into the soil and chemical defence inthe form of calcium oxalate in the leaves, while com-pensatory re-growth of bulb and leaves from the basalmeristem can be interpreted as a form of tolerance.
If hysteranthous geophytes change their allocationof resources according to herbivore pressure, selectionmay act on P. sickenbergeri populations with lowresource availability and exposed to constantly highherbivory, to minimize the cost of lost tissue and gen-erate an efficient system of resource allocation. Wetested for this by investigating whether removing dif-ferent amounts of bulb tissue affects investment ingrowth and bulb defence and the effect of this invest-ment on fitness as measured by the plants futuregrowth and reproductive performance. We predictedthat as the amount of bulb removed increases (up toa certain threshold), plants would increase their re-growth capacity to compensate for the damage. Plantsthat exhibit such a tolerant strategy will not have areduction in fitness, whereas avoidance of herbivory byinvestment in defence would results in trade-offs being
evident between this investment and other plant func-tions such as storage, growth and reproduction.
Materials and methods
The study was conducted in Makhtesh Ramon, ananticlinal 200 km2 erosion cirque with low rainfall (4090 mm per year) situated on the southern boundary ofthe Negev Desert, Israel (see Saltz et al. 1999). Thehigh variance in annual rainfall and temperature arereflected in the vegetation (Ward & Olsvig-Whittaker1993; Ward et al. 1993; Saltz et al. 1999). We concen-trated this study in Machmal dune, along the easterncliffs of the cirque, where plants of P. sickenbergerisuffer the highest level of herbivory. Loose sands cansupport dense populations of these lilies (up to 2 m2),which attract dorcas gazelles (Ward & Saltz 1994; Saltz& Ward 2000).
P. sickenbergeri blooms in the autumn. Leaves appearafter the flowers have wilted (hysteranthy), in responseto winter rains in late November and December, andmay remain green until late spring, depending on rain-fall and temperature. In spring, all the leaves dry up andfall off, leaving no above-ground material (Saltz &Ward 2000). During winter, gazelles eat the leaf tips(the terminal centimetre or so) and up to 100% of theplants may be affected. The tip is the only part of theleaf not defended by needle-like raphides of calciumoxalate, suggesting that this chemical is an effectivedeterrent to this herbivore (Ward & Saltz 1994; Wardet al. 1997; Saltz & Ward 2000). Because the leaves havea basal meristem (Bold et al. 1987) their growing pointis not affected by gazelle herbivory (Ward & Saltz1994).
During the summer gazelles dig up and consume allor part of the P. sickenbergeri bulbs. Bulbs that arepartly consumed have a lower probability of producingflowers and leaves the following winter and leaves thatare produced are fewer and smaller (Ward & Saltz1994; Saltz & Ward 2000). These correlations suggestthat, at least in the short term, there is an effect of bulbherbivory on plant fitness. The greatest impact thegazelles have on P. sickenbergeri populations in sanddunes is the consumption of flowers. Although eachplant produces one to two stalks (220 cm) with two toten flowers (612 cm) on each and each fruit (27 cm3)can produce many (50200) relatively large wind-dispersed seeds (610 mm, 0.5 4.0 g), inflorescences inthis environment have less than a 0.0001 probability ofsurviving to seed-production (Saltz & Ward 2000). Anysurviving seeds germinate after the winter rains andleaves are produced. A bulb then develops that growslarger and deeper with time (Ward & Saltz 1994).Within populations, all morphological characteristics
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2002 British Ecological Society, Journal of Ecology, 90, 472479
are allometrically scaled to one another. There aresignificant positive correlations between depth of thebulb, bulb volume, shaft diameter, leaf diameter, leafnumber and plant wet mass (Ward & Saltz 1994).
The dorcas gazelle is a small herbivore native tothe deserts of southern Israel and the Middle East.Gazelles show a number of behavioural characteristicsconsistent with a long period of coadaptation with theP. sickenbergeri. In the winter they select the biggestplants with the most leaves, consuming only the calciumoxalate-free leaf tips. Summer foraging is optimized bydigging for those plants that maximize the benefit : costratio, which is influenced by the depth of the bulb andthe degree of sand compaction (Ward & Saltz 1994;Saltz & Ward 2000).
During the summer of 1996 we measured the initialsize (bulb diameter) of 80 bulbs in the population atMachmal dune and randomly assigned 20 plants toeach of four bulb-cutting treatments: control (noremoval), transverse cut at the top (25% removed), cuthalfway down the bulb (50% removed) and cut at thebase (75% removed). The cutting was done in situwithout removing the bulb, to avoid root disturbanceor damage, and the plants were then fenced to protectthem from subsequent gazelle herbivory. The follow-ing growing season (January 1997) we determinedthe effects of cutting on leaf growth by counting thenumber of leaves per plant and measuring length andwidth of the leaves. To establish the effect of the cuttingtreatments on the reproductive performance of theplant, we measured flower stalk height, number offlowers, number of fruits, fruit volume, number ofaborted fruits and number of seeds per fruit duringthe flowering season (October to November 1997). Inthe flowering season of 1998 we counted the number offlowers, number of fruits and number of aborted fruitsper plant. In 1999 we measured flower stalk height,number of fruits, number of aborted fruits and numberof seeds per plant. We used the number of fruits and thenumber of seeds as estimates of current fitness.
To determine the effects of cutting on bulb size,growth, storage and defence, we collected all the bulbsat the end of the 1999 flowering season and measuredtheir diameter, fresh weight, dry weight, net growth andenergetic content. Energetic content was used as anapproximation of total stored carbohydrate in the bulbor the energy available to support plant functions.Energy was measured using an oxygen bomb calori-meter (Parr) and the total energetic content was calcu-lated per unit total dry weight of the bulb. Bulb netgrowth is an estimate of the capacity of the plant tocompensate after damage. It was calculated as:
Bulb net growth = Bulb diameterfinal (Bulb diameterinitial Percentage bulb removed Bulb diameterinitial)
We also determined total oxalate as a proportion ofbulb mass and shaft length.
P. sickenbergeri bulbs produce crystals of calciumoxalate, which may be a chemical defence against bulbherbivory (see Ward et al. 1997 for description of therole of calcium oxalate in leaf defence). Percentageoxalate in the bulb was estimated by measuring thepercentage of oxalate in 1.5 g of dry bulb tissue, usinga total oxalate assay (Moir 1953).
After testing for normal distributions with aKolmogorov-Smirnov test, all variables were log10-transformed. The effect of the cutting treatment onvegetative growth, reproduction, storage and defencewas analysed by , with bulb size prior to cutting(initial bulb diameter) used as a covariate. To facilitatefluent reading, we omit log10 at the beginning of thevariable name, except where it is part of the results. The relationship between variables was estim-ated with a simple regression model. The probability ofproducing leaves and flowering each year was estimateby a 2 test ( 7).
The proportion of bulbs producing leaves in the grow-ing season following simulated herbivory (6 monthslater) was significantly different between treatments(2 = 42.16; P < 0.0001). Bulbs that were cut at thebase (75% of the bulb removed) had the lowest prob-ability of leaf production (3 of the 20 plants), while allcontrol plants produced leaves, and 12 and 19 plants,respectively, produced leaves following 25% and 50%cuts. We also found a significant effect of the cuttingtreatment on the number of leaves that plants producedin the next growing season (1997) when we used initiallog10 bulb diameter as a covariate (F = 29.3, P < 0.001,error d.f. = 75). A similar result was achieved whenwe used the current plant size in 1997 as the depend-ent variable (F = 4.5, P = 0.005, error d.f. = 75,covariate = log10 leaf width size). Cutting treatmenthad a significant effect on leaf length (F = 25.98,P < 0.001, error d.f. = 75, covariate = log10 initial bulbdiameter) and leaf width in that season (F = 22.52,P < 0.001, error d.f. = 75, covariate = log10 initial bulbdiameter). In general, plants in the base- and top-cuttreatments (75% and 25%) had lower mean values thanplants in half-cut and control treatments. Bulbs in theextreme cutting treatment...