Predispersal reproductive ecology of an arid landcrucifer, Moricandia moricandioides: effect of

mammal herbivory on seed production

Jose M. Gomez

Departamento Biologıa Animal y Ecología, Facultad de Ciencias,Universidad de Granada, 18001 Granada, Spain

(Received 10 February 1995, accepted 13 March 1995)

In this paper the effect of herbivory on the seed production of Moricandiamoricandioides (Cruciferae), an annual species living in arid habitats of south-eastern Spain, is analysed. Firstly, the flowering and fruiting phenology andthe composition and structure of the pollinator guild is described, in order tocompare the overall effect of mutualistic species vs. that of antagonisticspecies on M. moricandioides seed production. The loss of female reproductivesuccess due to each herbivore species attacking the plant is then quantified, inan attempt to differentiate the effects on plant seed production of eachherbivorous species. The results indicate that only antagonistic organismsinteracting with M. moricandioides influenced the female fitness of this plantspecies. In fact, pollinator abundance or activity did not correlate with thenumber of seeds dispersed by the plants. In addition, of all the herbivorespecies, only sheep activity significantly influenced seed production of M.moricandioides individuals, the effect of the remaining crucivorous herbivoresbeing cancelled by the stronger herbivory of sheep. The results of this studysuggest that herbivory by sheep, in addition to decreasing the seed productionof M. moricandioides, could be an important determinant of the currentdistribution pattern of this crucifer species on the ramblas of the Bazabasin.

©1996 Academic Press Limited

Keywords: Cruciferae; Moricandia moricandioides; mammal herbivory; aridlands; Spain; seed production; predispersal plant ecology; animal–plantinteraction

Introduction

Herbivory is considered an important factor determining the fitness of large numbersof plant species (see reviews by Crawley (1983) and Fritz & Simms (1992)). Indeed,herbivores dramatically decrease the seed or fruit production (Marquis & Alexander1992), the competitive capacity (Ritchie & Tilman, 1992), the capacity for asexualreproduction (Cain et al., 1991) and the distribution area (Boyd, 1988; Herrera, C.M., 1990; Herrera, J., 1991) in many plant species. In addition, herbivores can affectthe diversity of plant communities, determining which plant species will be dominant

Journal of Arid Environments (1996) 33: 425–437

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in these communities (Ritchie & Tilman, 1992). As a consequence, it is hypothesizedthat herbivores frequently exert a strong selective pressure on plant species (Marquis,1992), causing the appearance of the many biochemical, morphological anddemographic traits displayed by plants in defense against consumers (Fritz & Simms,1992). However, the idea of selective pressure by a herbivore is complicated by the factthat plants normally interact with more than one animal species, and in most caseseach herbivore imposes opposite selective pressures on plants (Simms & Rausher,1989; Simms, 1990). Futuyma (1983) has noted that the fauna of most plants iscomposed of many polyphagous, apparently non-coevolved species and severalspecialized species. In these systems, the action of the non-specialist herbivores maycancel the possible selective effect of the specialists (Duggan, 1985). In several cases,the potential for evolution between animals and plants may depend upon thecommunity context in which the interaction takes place rather than the outcome of thepairwise interaction (Thompson & Pellmyr, 1992; Herrera, 1993).

In Cruciferae, it is commonly accepted that the heaviest damage normally resultsfrom attacks by adapted herbivores, because crucifers have a glucosinolate–myrosinasesystem that acts as a defence principally against generalist herbivore species (Blau et al.,1978; Chew, 1988). In fact, it is generally assumed that glucosinolates are toxic tomost non-cruciferous insects (Kirk, 1992). However, most studies on herbivory inCruciferae have considered only the effect of insects, and/or the chemical-typedefenses of the plants (Chew, 1988; Renwick, 1988; Agren & Schemske, 1993). Butseveral species of crucifers are frequently eaten by mammals (Duggan, 1985; Delph,1986; Dieringer, 1991; Gedge & Maun, 1992; Milchunas et al., 1992; Gomez, 1993).In most cases, mammal responses to secondary compounds are very different fromthose of insect species (Lindroth, 1988, 1989), and the chemical defense used to deterinsect herbivores may be ineffective against mammals.

Moricandia moricandioides (Boiss.) Heywood (Cruciferae) is an annual cruciferspecies living in arid habitats of south-eastern Spain largely used for livestock. In thispaper, factors affecting seed production of this plant species during one breedingperiod are analysed. The main goal is to quantify the composition and abundance ofthe pollinator assemblage as well as the herbivore feeding on this plant. The loss offemale reproductive success due to each herbivore species attacking this plant speciesis quantified, in order to compare the overall effect of the mutualistic species vs. thatof the antagonist species on seed production.

Methods

Study area

The study was carried out during 1991 in Rambla del Espartal, a seasonal watercourse(rambla) near Baza (Granada, SE Spain). The substrate is composed of silt withgypsum sediments, forming a typical badlands landscape, with the bed of thewatercourse surrounded by steep hills. The arid climate has an annual rainfall of300 mm, which is usually irregularly distributed from October to April, with a total of70 rainy days per year, 45–50% of these registering less than 10 mm m–2 of rain.During the study year (1991) annual rainfall in Baza was 281 mm m–2 (Hodar, 1993).Potential evapo-transpiration is three times the annual rainfall. Annual average soiltemperature is 14·4°C.

The vegetation is a typically arid open shrub–steppe, with species such as Retamasphaerocarpa (L.) Boiss., Seriphidium herba-alba (Asso.,) Y. R. Ling, Ononis tridentataL., Salsola vermiculata L., Gypsophyla struthium L. and Lepidium subulatum L. There isa 27% shrub coverage with 22% grassland and 40% bare soils (Hodar, 1993). In this

J. M. GOMEZ 426

area, M. moricandioides usually grows only on the upper part of the hills and on thesteepest slopes, only occasionally growing on the soft slopes.

Study of flowering phenology and floral morphometry

For this study, a M. moricandioides population (c. 90 plants) consisting of plantsoccupying two microhabitats, the slope and the top of the hill surrounding thewatercourse, was selected. The flowering phenology of this species was determined bycomparing, throughout the reproductive season, the number of plants in flower withrespect to the total number of plants in the population. At the beginning of theflowering period, 30 plants were randomly labelled, 15 of them growing on a gentleslope (‘slope’, hereafter) and the remaining 15 growing on the upper part of the hill(‘top’, hereafter), and all newly opened flowers were measured. Measurements taken(in mm) were petal length, length between the corolla–peduncle insertion and the petalbase (corolla tube length, hereafter) and the major diameter of the flower (corollawidth, hereafter). All measurement were made using a digital caliber. In total, 189 M.moricandioides flowers were measured.

Censusing of pollinators and herbivores and plant reproductive success

The composition and abundance of the pollinator assemblage was assessed during theperiod of maximum flowering, using 2-min censuses in which all the insects visiting theflowers of labelled plants were counted. Censuses were taken periodically throughoutthe flowering peak. During the study period, 420 2-min censuses (14 h of netobservation) were made, giving an average of 14 censuses per plant. Pollinatorabundance was expressed as the number of insects per 60 min of observation. Anyinsect seen on the flowers that could make contact with the anther and/or stigma wasconsidered to be a flower pollinator. The foraging pollinator behaviour of the mostabundant pollinator species, bees, was studied, quantifying the number of flowersconsecutively visited in each labelled plant before leaving it. The observations weremade at approximately 1 m from the plants to avoid altering the normal behaviour ofthe pollinators.

The effect of each herbivore species was quantified by periodically counting thenumber of flowers, fruit and leaves attacked by animals, and identifying the herbivores.By means of periodic direct observations, it was possible to distinguish the effect ofeach herbivore species on plant tissues. In total, four types of herbivores wereobserved: invertebrate floral herbivores, invertebrate folivores, vertebrate floral andfruit eaters, and seed predators. To test whether the invertebrate floral herbivores infact affect the female productive success of the plant 15 damaged flowers were labelled.In all cases, the attacked flowers abscided without producing fruit. The intensity ofherbivores attacking reproductive tissues (flower, fruit and seeds) was estimated bydividing the number of items eaten by the total number of items available. However,the intensity of herbivores attacking vegetative tissues (principally leaves) wasestimated by counting the number of leaves attacked and the proportion of these eatenby the herbivores.

During the censuses, the height of each plant and the number of opened flowers,floral buds and fruits were also quantified. The total number of flowers per plant (floraldisplay) was determined by adding the number of flowers, floral buds and fruitexhibited by each plant. At the end of the fruiting period, before seed dispersal, allplants were collected, and the number and position of mature fruits determined,working up from the base to the top of the stalk. Every mature fruit was taken to thelab to count the number of ovules, intact seeds and depredated seeds. It was easy to

SEED PRODUCTION OF MORICANDIA MORICANDIOIDES 427

distinguish ovules from ripe seeds, since morphologically they clearly differ. In total,251 fruits and 11,999 seeds were analysed.

To estimate the female reproductive success of the plants, three rate-basedcomponents have been used: fruit set (proportion of flowers setting mature fruits);seed/ovule ratio (the proportion of ovules setting seeds in each mature fruit); andfemale fertility, this last parameter being quantified by multiplying the first two(Charlesworth, 1989). In addition, because of the problem of using only relativeestimates of fitness (Herrera, C. M., 1991), the total fecundity of the plants, i.e. totalnumbers of seeds dispersed by each labelled plant, has been also quantified.

Statistical analyses

To determine bivariate relationships between pollinator or herbivore activities and theestimates of plant reproductive success, non-parametric correlations (Spearman rankcorrelation) were used. However, several phenotypic variables are discrete (forexample, microhabitat). In these cases, an analysis of variance was performed,previously testing the equality of variances by using a Levenne test. If the two groupshad significantly different variances, the means were tested using a Welch F-test, thatallowed S.D. are not equal.

To appreciate the overall effect of all variables on the reproductive success, a generallinear model was fitted using as dependent variables fruit set or fecundity, and asindependent variables those which proved to be significantly related to reproductivesuccess, according to bivariate tests. In these parametric analyses, the variableexpressed as a ratio were arcsine transformed and the others were log-transformed(Zar, 1984). Type III sum of square was consistently used, due to the unbalancednature of the data (Shaw & Mitchell-Olds, 1993).

Results

Reproductive traits: phenology, size and floral display

Moricandia moricandioides plants in the studied population produced a basal rosette ofleaves, with an average ( ± 1 SE) of 4·87 ± 1·12 (range: 0–12) leaves per plant and 1to 8 stalks per plant (mean ± 1 SD: 2·60 ± 1·90). Individuals can grow to 61 cm inheight, with a average ( ± 1 SE) of 37·93 ± 1·75 cm. There was no difference in plantheight depending on microhabitat (p > 0·7, one-way ANOVA).

Flowering in this species lasted c. 2 months, from the first few days of April to thelast day of May (Fig. 1). In 1991 the flowering peak occurred on 19 May (Fig. 1). Onthis date, more than 60% of the plants were in flower. The individuals of this speciesat the study site flower more or less synchronously. Throughout the flowering season,the labelled plants produced an average ( ± 1 SE) of 63·4 ± 11·21 flowers, with someplants producing only six flowers and others as many as 334 (Fig. 2). There was astatistical difference in the number of flowers depending on microhabitat (F = 7·74,df. = 1·28, p = 0·01), with plants on the slope displaying almost double the number offlowers compared to plants on the top of the hill (84·72 ± 19·82 vs. 42·07 ± 7·91flowers; mean ± 1 SE). However, during the flowering peak, only 11·6 ± 1·75(mean ± 1 SE) flowers were open per plant (range 1–49). Fruit production began veryearly, in the first few days of flowering, around 6 April (Fig. 1).

The purple–violet flowers of this crucifer were 15·96 ± 0·26 mm in width, withpetals 7·51 ± 0·15 mm in length and a corolla tube 12·36 ± 0·16 mm in length (Table1). As shown in Table 1, there is a strong correlation between these floral traits(p < 0·001 all pairwise Pearson correlations). In addition, there was inter-microhabitat

J. M. GOMEZ 428

30 May

60

01 April

Date

Per

cen

tage

of

plan

ts in

flo

wer

10 May

50

40

30

20

10

6 April 13 April 19 April 27 April 20 May

100

0

80

60

40

20

Cu

mu

lati

ve p

erce

nta

ge o

f fr

uit

s

14

0Number of flowers per plant

Nu

mbe

r of

pla

nts

20050 150

10

12

8

6

4

2

100 250 300 3500

Table 1. Descriptive statistics of each floral trait considered. Also shown is thecorrelation–covariance matrix among floral traits (figures above diagonal are

covariances and figures below diagonal are correlations)

Correlation–covariance matrix

CorollaPetal Corolla tube

Floral traits Mean±1 SE Range CV length width length

Petal length 7·51±0·15 6·19– 9·30 11·25 1 1·083 0·543Corolla width 15·96±0·26 13·78±20·04 9·03 0·890 1 0·821Corolla tube

length 12·36±0·16 10·31±14·00 7·23 0·719 0·637 1

Figure 1. Flowering (h) and fruiting (d) phenology in Moricandia moricandioides.

Figure 2. Frequency distribution of number of flowers per plant (n = 30 plants) in M.moricandioides.

SEED PRODUCTION OF MORICANDIA MORICANDIOIDES 429

Table 2. Abundance of insects visiting M. moricandioides flowers in 1991,showing mean abundance (expressed as number of insects per census), range ofeach species counted in one census and the percentage that each insect species

represents with respect to total insect visits

Species (Family) Mean±S.D. Range %

Anthophora romandii Lep. (Anthophoridae) 4·000±1·148 0–17 72·74Eucera nigrilabris Lep. (Anthophoridae) 0·714±0·438 0–5 12·98Melecta sp. (Anthophoridae) 0·286±0·163 0–2 5·20Lassioglossum albomaculata Lac. 0·286±0·611 0–2 5·20

(Halictidae)Andrena sp. (Andrenidae) 0·071±0·267 0–1 1·59Dasytidae 0·071±0·267 0–1 1·59

19

10

–19

Hour of the day

Nu

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per

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14

43210

10 11 12 13 15 16 17 18

56789

differences in all floral morphometric traits. Flowers from the slope were bigger,16·44 ± 0·3 mm in width, with petals 7·84 ± 0·2 mm in length and a corolla tube12·69 ± 0·27 mm in length, than the flowers from the top, that were 15·47 ± 0·4 mmin width (F = 4·29, p = 0·05), with petals 7·17 ± 0·21 mm in length (F = 5·66,p = 0·02) and corolla tube 12·03 ± 0·15 mm in length (F = 4·14, p = 0·05).

Pollinator assemblage

Flowers of this crucifer were visited during 1991 by only six species of insects (Table2). However, Halictidae and Dasytidae were too small for consistent contact with thestigma while foraging, and for this reason it was assumed that only andrenids andanthoforids were true pollinators. The most abundant species was Anthophora romandiiLep., which represented more than 70% of the flower visitors during the study period.In general, the three species of anthoforids registered in M. moricandioides flowersaccounted for more than 90% of the flower visits.

The average ( ± 1 SE) abundance of insects in M. moricandioides flowers was4·5 ± 0·79 insects per census. Abundance of pollinators was greater at midday (Fig.3), a significant relationship appearing between the hour of the day and the number ofinsects per census (F = 9·91, df. = 2·11, p = 0·003, R2 = 0·64). There was no

Figure 3. Daily activity of pollinators in M. moricandoides, showing the number of insects percensus (60 min) according to the hour of the day. The quadratic regression equation isy = –63·34 + 10·35x –0·38x2 (F = 9·91, df. = 2·11, p = 0·035, R2 = 0·58 for the quadraticregression equation).

J. M. GOMEZ 430

significant difference in the abundance of pollinators depending on the microhabitatoccupied by the plants (F = 2·28, df. = 1·28, p = 0·14).

There was no relationship between floral trait and insect visitation rate (p > 0·1 forthe three floral traits, Spearman rank correlation). Nor was there any apparentrelationship between plant height and insect abundance per plant (p > 0·1), Spearmanrank correlation). The only phenotypic trait which was related to insect visitation ratewas the number of flowers displayed by each plant — plants with more flowers werevisited by more insects than plants with fewer flowers (rs = 0·43, p = 0·02).

The average number ( ± 1 SE) of flowers consecutively visited in each plant by A.romandii was 1·57 ( ± 0·10), ranging from plants in which bees visited only one flowerand plants in which bees visited three flowers per each foraging bout. If we assumethat, during flowering peak, an average plant has 12 open flowers, each time beesvisited 13% of the available flowers. The number of flowers visited by bees did notdepend on any of the floral morphometric traits (p > 0·8 in all cases, Spearman Rankcorrelation).

Herbivory on flowers, fruits, seeds and leaves

Flowers of M. moricandioides were eaten by one species of Tenthredinidae (possiblyTenthredo sp.). Of the 30 labelled plants, 54% were attacked by this floral herbivore.This wasp makes a hole in the base of the flower corolla, ingesting the ovary andstamens. The average ( ± 1 SE) number of flowers eaten per plant in 1991 was1·27 ± 0·29 (range: 0–6); that is, 2% of available flowers. There were no relationshipsbetween floral herbivory pressure and flower number per plant (p > 0·05, Spearmanrank correlation). However, floral herbivores did select plants with smaller flowers. Infact, there was a negative relationship between floral herbivory pressure and petallength (rs = –0·276, p < 0·05) or corolla tube length (rs = –0·294, p < 0·05). Flowersof M. moricandiodes are also occasionally attacked by a beetle species, Mylabrismaculosopunctata Graells (Meloidae; Sanchez-Pinero, pers. comm.), but this beetle isa very rare predator of this plant species and it did not appear in the censuses.

The flowering stalks of M. moricandioides were grazed by domestic sheep, whichingested principally flowers. The effect of this mammal was dramatic; the stalks of all15 labelled plants growing on the slope microhabitat were completely eaten, and66·82% of the flowers and fruits of the total labelled plants were lost to theseherbivores. Although overcompensation has been observed in plants at other sites,grazed plants in this study did not produce any seeds after mammal herbivory. Heighthad no effect on whether plants were grazed or ungrazed (p > 0·1, one way ANOVA).The only significant factor was microhabitat; only plants growing on the slope weregrazed by sheep.

Only Pieris brassicae L. (Pieridae) was observed living on the leaves and thus, it wasassumed that folivory is due principally to this butterfly, which attacked 73% of theplants ungrazed by sheep. The average number ( ± 1 SE) of leaves attacked per plantwas 2·4 ± 0·58 (range: 0–7). In total, folivores ate 16·88% ( ± 5·62) of leaf biomass(range: 0–70%). The intensity of folivory did not depend on the number of leaves perplant (p > 0·1, Spearman rank correlation).

Finally, the seeds of M. moricandioides were eaten by a microlepidoptera species,which attacked 60% of the 15 plants ungrazed by sheep, killing 6·3 ± 0·9% ( ± 1 SE)of seeds per fruit, and eating 3·20 ± 0·48 seeds per fruit (range: 0–44). However, asshown in Fig. 4, more than 80% of the fruit were not attacked by this insect. Thenumber of depredated seeds significantly increased with plant height (rs = 0.561,p = 0·03, n = 15 plants) and fruit size (rs = 0·21, p = 0·001, n = 245 fruits). Norelationship appeared between the remaining plant phenotypic traits and intensity ofseed predation (p > 0·05, Spearman rank correlation). Nor was there any relationship

SEED PRODUCTION OF MORICANDIA MORICANDIOIDES 431

100

0

No. of depredated seeds per fruit

Per

cen

tage

of

fru

its

11–150 6–10

80

60

40

20

1–5 16–20 21–25 26–35 36–45

Table 3. Effect of phenotypic traits on fruit set. Only variables with significantcorrelation (p<0·05) were included in the linear model

d f. SS F p

Petal length 1 0·000 0·000 0·989Corolla tube length 1 0·000 0·018 0·895Floral display 1 0·001 0·051 0·822Microhabitat 1 0·958 78·706 0·001Residual 25 0·304

df. = degree of freedom; SS = Type III sum of square; F = F-ratio statistic.

between intensity of seed predation and flower position on the stalks (p > 0·05,Spearman rank correlation).

Estimates of reproductive success: effect of size, pollinators and herbivores

The fruit set was 20·7 ± 4·3 (range: 0–72·2%), although 50% of plants did not set anyfruit. The probability that a flower ripened to fruit depended on its position on thestalk (Chi-square = 38·05, p = 0·00001, n = 630 flowers, Logistic regression), withflowers situated on the lower part of the stalk having a greater probability of settingfruit than flowers arranged on the upper parts. Microhabitat, floral display, petal lengthand corolla tube length were the only traits significantly related to fruit set (p < 0·05all bivariate relationships, Spearman rank correlation). To determine which factorsaffect this fitness component, these traits were introduced into a general linear model.This model explained 80·9% of the variability in dependent variable (F = 26·402,df. = 4,25, p = 0·0001). As can be observed in Table 3, only microhabitat significantlyaffected M. moricandioides fruit set: plants growing on slope produced no fruit, whereasplants growing on the top set an average ( ± 1 SE) of 41·4% ( ± 3·8) of flowers. Thismicrohabitat effect was exclusively due to sheep grazing on plants living on the slope(see above).

The seed/ovule ratio was the other relative fecundity component analysed for M.moricandioides. The number of ovules per flower ( ± 1 SE) was 48·20 ± 1·06, with amaximum of 88. The number of seeds per mature fruit was 36·08 ± 1·36, up to 84seeds per fruit. The average ( ± 1 SE) percentage of ovules producing ripe seeds per

Figure 4. Frequency distribution for the number of seeds depredated by microlepidopters ineach ripe fruit (n = 15 plants).

J. M. GOMEZ 432

13.25

1

011

Corolla tube length (mm)

See

d/O

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rat

io

12.25

0.40.30.20.1

11.25 11.5 11.75 12 12.5 12.75 13

0.50.60.70.80.9

20

0

Fecundity

Nu

mbe

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nts

800200 600

1012

8642

400 1000 1200 20001400 1600 18000

141618

mature fruit was 74·9% ± 7·2 (range: 8·6–97·4%). Only corolla tube length wasrelated with this fitness component (rs = 0·59, p = 0·027). The relationship betweenthis reproductive success estimate and floral morphometric trait was fitted by means ofa quadratic regression equation (Fig. 5); in general plants with larger corolla tubesproduced more seeds per fruit.

Female fertility (the proportion of total ovules setting seeds per plant) wasdetermined by combining fruit set and seed/ovule ratio. The average female fertility( ± 1 SE) was 15·4% ( ± 3·6), ranging from plants with 0 to 62·7% of their ovulessetting seeds. Average female fertility in plants not eaten by sheep was 30·9 ± 4·5%.No trait was statistically related to this estimate of female productive success, exceptmicrohabitat (F = 47·4, p = 0·0001, Welch test): female fertility of plants on the slopewas 0, whereas the average female fertility ( ± 1 SE) of plants of the top was30·9 ± 4·5%.

The average ( ± 1 SE) fecundity of the plant was 299 seeds ( ± 88), ranging fromplants that dispersed no seeds to plants that dispersed more than 1800 seeds (Fig. 6).Most plants, however, by the end of the fruiting period dispersed less than 200 seeds(Fig. 6). Plants not eaten by sheep dispersed 599 ± 140 seeds. Fecundity was relatedonly to the number of flowers displayed per plant; smaller plants dispersing more

Figure 5. Relationship between corolla tube length and percentage of ovules ripening seeds permature fruit in each labelled plant. Each dot represents one plant. The quadratic regressionequation is y = –71·02 + 11·59x – 0·47x2 (F = 13·73, df. = 2,14, p = 0·0008, R2 = 0·70 forthe quadratic regression equation).

Figure 6. Frequency distribution for the number of seeds dispersed per plant (fecundity).

SEED PRODUCTION OF MORICANDIA MORICANDIOIDES 433

Table 4. Effect of phenotypic traits on fecundity. Only variables with significantcorrelation (p<0·05) were included in the linear model

d f. SS F p

Floral display 1 297897 2.108 0·158Microhabitat 1 2982957 21.111 0·001Residual 25 3815154

df. = degree of freedom; SS = Type III sum of square; F = F-ratio statistic.

seeds, (rs = –0·458, p = 0·003), and with microhabitat; plants growing on the slopedispersed no seeds due to sheep herbivory, whereas plants living on the top dispersed599 ± 140 (mean ± SE) seeds (F = 20·79, df. = 1,28, p < 0·0001; Welch F-test).But, when these variables were introduced in a general linear model, only microhabitatsignificantly influenced plant fecundity (Table 4), this model explaining 70% of thevariability in the dependent variable (F = 15·40, p = 0·0001).

Discussion

The results suggest that only antagonistic organisms interacting with M. moricandioidesinfluence female fitness of this plant species. In fact, both pollinator abundance oractivity did not correlate with the number of seeds dispersed by the plants. Nor wasthere any relationship between floral traits and pollinator abundance, indicating thatthe possibility for selective pressure by bees on floral morphology is too weak.

Moricandia moricandioides was eaten during 1991 in the study area by at least threespecies of phytophagous insects and one species of mammal herbivore. However, onlymammal herbivory significantly influenced seed production by M. moricandioidesindividuals, the effect of the remaining herbivorous species being cancelled by thisstronger herbivory by sheep. This occurred despite virtually all the plants having beenattacked by the three remaining species of herbivores. It was assumed that, as in othersystems where one plant species is eaten by several very different herbivorous species(e.g. Gomez, 1993), the large size of the sheep makes it important as a herbivore forthe plant species. Thus, due to all the above-mentioned reasons, there appears to bea strongly structured system of herbivores eating M. moricandioides, in which onespecies, the sheep, may influence not only plant fitness but also the interactionsbetween the plant and the insect herbivores.

Moreover, according to our results, the main herbivore of M. moricandioides during1991 was a generalist mammal herbivore not adapted to crucifers, in spite ofLockwood & Belkhiri (1991) having shown the occurrence of at least methionine-derived, phenylalanine-derived and tryptophan-derived glucosinolates in the leaves ofspecies belonging to the genus Moricandia. In addition, the effects of Pierisbrassicae — a specialist herbivore of crucifers (Chew, 1988; Lamb, 1989; Kirk, 1992)which lays clutches of eggs and the larvae rapidly defoliate individual hosts includingMoricandia arvensis (L.) DC. (Courtney & Chew, 1987) — on M. moricandioides seedproduction was almost negligible. In this context, the potential phenotypic selectionmediated by a specialist herbivore, for example Pieris brassicae, on M. moricandioidesevolution would currently be cancelled by the stronger herbivory of generalistmammals, such as the sheep. The effect of P. brassicae on plant fitness wouldpresumably be apparent only in plant populations in which sheep were rare. Thisstatement is important in the Mediterranean basin where livestock raising has been animportant activity for over 2000 years.

The severe effect of sheep grazing on M. moricandioides may have immediate

J. M. GOMEZ 434

consequences. Firstly, population dynamics of this crucifer can be affected by thisherbivory pressure. Indeed, half of the plant population produced no seeds in 1991.Several authors have shown that in arid habitats, mammal herbivory can be a majorfactor in the population biology and fitness of plant species (e.g. Waser & Price, 1981;Inouye, 1991; Auld, 1993; Kerley et al., 1993). The negative effect on plantpopulations of mammal herbivory, both domestic and wild species, has also beenreported variously in other habitats of southern Spain (Herrera, 1990, 1993; Herrera,J., 1991). However, there is no consensus on the long-term effect of mammalherbivory on arid plant population dynamics (Inouye, 1991), and the present studyconsiders only one reproductive event.

Secondly, due to the foraging behaviour of sheep, neither floral traits nor plantheight correlated with the number of seeds dispersed by the plants. In addition, the sizeor number of flowers produced by the plants throughout the reproductive season(floral display) did not affect the total number of seeds dispersed by M. moricandioides,a typical phenotypic trait that determines the fecundity and relative fitness ofindividuals in other plant species (Herrera, C. M., 1991; Stanton et al., 1991; VanTienderen & Van der Toorn, 1991; Andersson, 1992; Klinkhamer et al., 1992). In thiscrucifer species the effect of sheep herbivory appears to be strong enough to cancel anyadvantage from producing many flowers.

Finally, of all traits analysed in this study, only the microhabitat occupied by theplants influenced the female fitness of M. moricandioides; the plants growing on theupper part of the hill dispersing many seeds because they were ungrazed by sheepwhereas the plants growing down on the slope dispersing no seeds, since only theseplants were grazed by sheep. If the habitat of the plant overlaps with that used bysheep, the probability of a plant being eaten dramatically increases. In the study areathe sheep normally forage in the bed of the watercourse and on the lower slopes, onlyoccasionally going up to the hill and normally only to cross from one rambla toanother. For this reason, M. moricandioides individuals growing on the top of the hillswould have a high survival probability. Curiously, in this area of the Baza basin, M.moricandioides usually grows on this upper part (pers. obs.), in spite of the fact that inthis microhabitat plants appear to produce fewer and smaller flowers than on the slope.This habitat-dependent survival has been reported for other species of plants,including several Chilenan species (Jaksic & Fuentes, 1980), Viola cazorlensis Grand.(Herrera, C. M., 1990, 1993), and Geranium purpureum Viii. (Herrera, J., 1991) inSpain, or Cakile maritima Scop. (Boyd, 1988) in the U.S.A., and in every case, in spiteof microclimatic conditions the distribution patterns appeared to be produced mainlyby mammal herbivory. Similarly, the results of this study suggest that herbivory bysheep, in addition to decreasing the seed production of M. moricandioides, could be animportant determinant of the current distribution pattern of this crucifer species on thearid lands of the Baza basin. However, further studies will be necessary to test theactual effect of mammal herbivory, with respect to other factors such as microclimateor seed dispersal, on the observed distribution pattern of this crucifer species.

I am most grateful to Francisco Sanchez-Pinero, Jose A. Hodar and Regino Zamora for theirhelpful suggestions. I also thank David Nesbitt for linguistic advice. Bee identifications weregenerously provided by Dr Javier Ortiz (University of Granada). This research was supported bya grant from P.F.P.I. and by a grant from DGICYT No. PB90-0852.

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