Factors affecting the dominance of Silybum marianum L. (Asteraceae) in its specific habitats.

Flora (1994) 189 201-206

© by Gustav Fischer Verlag Jena

Factors affecting the dominance of Silyhum marianum L. ( Asteraceae) in its specific habitats. RAKEFET GABAyh, UZI PLITMANN 1 and AVINOAM DANIN2 Accepted: February 6, 1994

Summary The annual Mediterranean thistle Silybum marianum L. is a synanthropic plant (i.e. related to human habitats) common in Israel. It dominates waste places and ants' nests, and is disseminated by wind and ants. The purpose of this study has been to find out some of the possible factors during the plant's life cycle, which may affect its dominance in its specific habitats. Our results show that: (1) There is no obvious allelopathic effect of S. marianum on the germination of other plants; (2) Its germinability is relatively high and not affected by removal of the elaiosome; (3) Thistle plants around the nests and in waste places are fast growing, have significantly higher biomass and more and larger heads than thistles in surrounding herbaceous habitats; (4) Where the thistles were removed, total number of companion species and their biomass have increased. The success of S. marianum may be primarily due to its aggressive vegetative growth, causing depression of adjacent species. Its seed production, achene dispersal modes, and germinability partly enhance its dominance. Ants' nests probably had been the primary habitats from which ruderal (nitrophilous) species, such as S. marianum, have invaded special man-made habitats. Key-words: Silybum marianum, dominance, biomass, species diversity, myrmecochory, primary and secondary habitats.

1. Introduction Silybum marianum (L.) GAERTNER is a common native annual thistle in the Mediterranean territory ofIsrael. The plant is regarded as ruderal or nitrophilous, forming dense stands at roadsides, waste places (KUPICHA 1975; FRANCO 1976; FEINBRUN-DQTHAN 1978; ALAVI 1983) and nests of the harvesting ants (Messar semirufus ANDRE) (DANIN & YOM-Tov 1990) where it grows in circles of 1- 2 meters in diameter. S. marianum is a myrmecochorous plant. Like many other myrmecochorous plants (BERG 1975; HANDEL 1978; BEATTIE & CULVER 1981; DAVIDSON & MORTON 1981; RICE & WESTOBY 1981; WESTOBY et al. 1991; PEAKALL et al. 1993), its dispersal units have an oily body (elaiosome). After removal of the elaiosome the units are discarded by the ants in the nest refuse zone and germinate there. Soil fertility in 1 2

Department of Botany, Department of Ecology, Systematics and Evolution, The Hebrew University, Jerusalem 91904, Israel.

ants' nests is high due to high content of organic material and nutrients combined with good aeration and higher absorbtion of water in such microhabitats (AVIDOV 1968; GENTRY & STIRITZ 1972; OFFER 1980; GLINSKY & STEPNIEWSKI 1985). DANIN & YOM-Tov (1990) showed that S. marianum plants growing in the refuse zones (which are nutrient enriched sites) are taller, have higher biomass and more inflorescences than plants growing far away. Plant communities at the nests contain just a few species. Formation of a nearly monospecific community might be related to adaptations expressed through the plant's life cycle. Allelopathic influence during the germination phase might account for the initial success of S. marianum. This phenomenon is known from other plants (MULLER 1966; FRIEDMAN et al. 1977; DATTA & CHATTERJEE 1980; RICE 1984). Further, strong vegetative growth of S. marianum through its growth phase may be at the expense of other plant species sharing this habitat. The aims of the present study have been to reveal some of the factors affecting the dominance of S. FLORA (1994) 189

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marianum in its specific habitats. Accordingly, the study is focused on germination and growth, assuming that a high germination rate combined with strong vegetative growth would enhance the competitive ability of S. marianum. Also, from analysis of the floristic composition of the specific habitats of S. marianum, ants' nests in particular, its primary habitats may be inferred.

2. Material and methods

2.1. Germinability and allelopathic effect (1) Germinability tests of S. marianum achenes included 3 treatments: (a) 300 mature achenes with elaiosomes, directly collected from plants; (b) 300 achenes collected in the refuse zone of ants' nests, all without elaiosomes; (c) 300 achenes, the elaiosomes of which were removed with forceps. All achenes were sown in petri dishes (100 achenes per dish). Germinated seeds were recorded each day. This experiment was carried out in two repetitions (total of 1800 achenes). (2) Possible allelopathic effects were determined in five treatments, each with two sets (light and dark) and 3 repetitions per treatment. Treatment 1 (control), (for each of the three replicates): Seeds of Erucaria rostrata, Beta vulgaris (cultivar) and S. marianum were sown in petri dishes, 30 seeds per dish. An equivalent set was placed in sealed boxes. Treatment 2: Five leaf pieces (0.15 g each) cut from S. marianum plants before the first rain (to avoid possible loss of allelochemicals) were put in a petri dish with distilled water for 24 h. The above species were sown around these pieces. Treatment 3: Leaf pieces (10 g) were soaked in 1 liter of distilled water for 24 h. Seeds were sown as before, and watered regularly with the extract. Treatment 4: Leaf pieces (10 g) were soaked in 1 liter of distilled water for 72 h. The extract was used to water the seeds. Treatment 5: 10 g of S. marianum leaves were ground thoroughly, then filtered with 1 liter of water. The sown seeds were watered with this extract. Number of seedlings and their development were recorded each day, for each of the treatments.

2.2. Productivity comparisons, diversity and vegetation composition 2.2.1. Studies within nests Fourteen ants' nests were located at two sites in Jerusalem, Judean hills: (1) Giva't Bet-Hakerem (35 11' E/31° 46' N): altitude - 750 m above sea level; soil - Terra-Rossa; vegetation - mostly of annual herbaceous plants, dominated by Avena sterilis, Hordeum spontaneum and Triticum dicoccoides with scattered trees of Styrax officinalis and Rhamnus lycioides subsp. graeca. (2) Talpiot 0

I

II

Ii,I ti

202

FLORA (1994) 189

(35 13' E/31° 45' N): altitude - 650 m above sea level; soil - Terra-Rossa; vegetation - annual herbaceous, dominated by Avena sterWs and Hordeum spontaneum. In both sites the climate is Mediterranean and mean annual precipitation is 660 mm. The circle of S. marianum (i.e. the refuse zone) around these nests was divided into two halves. In one half all above ground parts of young S. marianum plants were harvested during the growing season ("Treated plots"). The second half remained intact and served as the control. After a month, the above-ground parts of all companion species were harvested from 0.5 x 0.5 m squares, one in the half of the refuse zone that served as the control and the other in the treated half; each sample was divided into subunits according to species. The subunits were oven-dried for 48 h at 90°C, then weighed. Rate of mass increase for each species was computed by dividing its mass in the control halves by its mass in the treated halves of the circle. Species diversity (eH ) was calculated using mass and number of species (HILL 1973). Most samples contained plants ofAvena sterilis, for which the number of spikelets (per inflorescence) was scored as well. 0

2.2.2. Studies in nutrient-rich sites and adjacent habitats Two sites were selected: (1) Abandoned field in the vicinity of Bet-Shemesh (34 57' E/31° 45' N), Judean foothills: altitude -210 m above sea level; mean annual precipitation - 450 mm; soil - Rendzina. This site is characterized by scattered ants' nests dominated by circles of S. marianum. (2) A site of garbage disposal 15 km west of Jerusalem (35 08' E/31° 45' N), Judean hills: altitude - 740 m above sea level; mean annual precipitation - 660 mm; soil Terra-Rossa. This site is a large abandoned waste place with nearly mono specific community of S. marianum. In both sites the climate is Mediterranean and the vegetation is mostly of herbaceous annuals with high abundance of Hordeum spontaneum. At site no. 1,0.5 x 0.5 m experimental plots were located in the refuse zone of five nests; five "control" plots were randomly located at least 5 m away from each nest, in the surrounding vegetation. At site no. 2, five plots were located in the waste place and five control plots at least 5 m away from its borders, among the natural vegetation. Variables of productivity measured for individual plants of S. marianum harvested in all plots were: height, dry mass, number of inflorescenes, receptacle diameter and number of achenes per head. Number of achenes per cm 2 of the receptacle and per plant were accordingly computed. Vegetation composition in each of the designated plots was determined by harvesting all the above-ground parts of the plants then separating the species for phytosociological analysis. Each species was oven-dried for 48 h at 90 and weighed. Species diversity (eH ) was calculated using mass and number of species (HILL 1973). 0

0

0

3. Results

3.1. Germinability and allelopathic effect (1) Germination started on the second day after sowing, in each of the three treatments. Mean values of germination at the 9th day were 30.5% for achenes with elaiosome and 30.8% for achenes without elaiosome. Germination rates were not significantly different (X 2 test, p > 0.05) between the treatments. (2) Allelopathic effects were examined by germinability of seeds of two species exposed to various extracts of S. marianum leaves. Germinability of seeds in the control was 98.8% and 76.2% for Erucaria rostrata and Beta vulgaris, respectively. Final percentages of germination on the 12th day in all treatments (Light: 98.8% -100% for E. rostrata; 74.1 % -78.6% for B. vulgaris. Dark: 86.5% to 99.7% forE. rostrata; 73.1 % -86.5% for B. vulgaris) were not significantly different from the control (X 2 tests with contingency tables, p > 0.01). All seedlings looked normal and no degeneration of seedlings was observed.

3.2. Biomass and diversity comparisons within nests Forty-three species were scored in the harvested samples from fourteen nests. Table 1 presents the mean values of number of species, biomass, and species diversity for plots with and without S. marianum. Number of species and diversity are higher in the treated plots (without S. marianum);

Table 1. Mean values of number, biomass and diversity of species in 14 halves of refuse zones (sites 1 & 2) with S. marianum intact compared with halves from which S. marianum had been removed. (One sided t-tests, * = significant at p < 0.025; ANOV A, * = difference significant at P :s:: 0.05). with S. marianum

without S. marianum

mean

S.D.

mean

S.D.

2.5

6.6*

2.3

18.9

49.8*

36.9

1.5

3.5

1.1

number of species /0.25 m 2 4.5* biomass gr/0.25 m 2 23.9* Species diversity (e H ) 2.9

Table. 2. Dry biomass of species common to nest halves with and without S. marianum. n = number of nests with species common to a plot and its control (two halves of a single nest). Average dry biomass (g)

Species

n plots with Silybum

Avena sterWs 8 14.3 Hordeum spontaneum 8 14.4 A vena barbata 3 3.5 Lolium rigidum 3 2.0 Hordeum glaucum 2 0.6 Aegilops peregrina 2 0.3 Bromus scoparius 1 0.4 Urospermum 1 1.5 picroides Picris sprengeriana 1 1.5 Carduus argentatus 1 3.6 Medicago poly1 0.1 morpha M edicago orbicularis 1 1.5 Onobrychis 1 0.3 squarrosa Erodium moschatum 2 1.0 Malva parviflora 2 3.4 Hirschfeldia incana 1 12.9 Cardaria draba 1 1.2

± 12.4

plots without Silybum 25.0

± 28.8

pro potional mass increase 1.7

± 14.9 17.9 ± 16.5 1.2 ± 3.2 6.4 ± 3.4 1.8 ± 1.5 16.9 ± 12.6 8.4 1.7 1.8 0.1

2.8 6.0 0.3

3.6 3.9 1.6

2.4 2.6 0.4

0.2

2.0

3.9

2.6

0.2 9.1 5.3 5.5 5.5

0.7 9.1 1.6 0.4 4.6

biomass of companion species is 2-fold higher in these plots. T -tests as well as ANOV A with two equal groups (at P ~ 0.05) showed that mean values of number of species and biomass differ significantly from the control. The increase in diversity was statistically not significant. Table 2 presents the 17 species common to control and treated plots (without S. marianum) of the same nest. The biomass of these species was higher by 1.2 to 9.1 times in the treated plots in 77% of the cases; in only four species (3 of which are ruderal plants) the biomass was reduced. The dominant grasses (A vena barbata, Avena sterilis and Hordeum spontaneum) were common to nest and control in 19 cases, in 16 of which the dry biomass was higher in the treated plots. However, t-tests showed no significant difference between the mean values of dry biomass in the treated and control plots for these grasses (data not shown). Likewise, the mean value of the number of spikelets of A vena sterilis in the control plots was 16.0 ± 8.54 (n = 30), and in FLORA (1994) 189

203

the treated plots 18.2 ± 8.47 (n = 38); t-test showed no significant difference between these groups.

3.3. Studies in nutrient-rich sites and the adjacent habitats Table 3 presents measures of morphological traits of S. marian urn plants from ants' nests and waste places vs. their respective controls. Height, number of flower heads per plant, receptacle diameter and mean number of achenes per head all have significantly higher values in plants of the nutrient-enriched sites, i.e. refuse zones of nests and waste places. The differences in height among sites were not significant (Fs for nests = 0.287, a = 5, n = 25; Fs for waste places = 1.2616, a = 5, n = 23). In these sites the Silybum plants reached their maximum height within

± 12 weeks, exceeding all the adjacent species and becoming twice as tall. Table 4 presents values of species number, biomass and species diversity per 0.5 x 0.5 m plots. Species number and diversity are significantly lower in refuse zones of nests and waste places than in the respective controls, whereas total biomass is higher (5 - 6 times). Both t-tests and single classification ANOV As reveal that the differences are statistically significant. Table 5 presents the distribution of species according to their characteristic vegetation types (after FEINBRUN-DoTHAN & DANIN 1991; DANIN, unpubl.). In the control plots of both locations, only 6% were synanthropic species (i.e. related to man-made habitats). In the refuse zone of nests and the waste places the percentages of synanthropic species were 25% and 50%, respectively. X2 tests showed significant differences in the frequency of synanthropic species between the controls and either of these nutrientenriched areas.

Table 3. Means (± standard deviation) of various productivity measures of S. marianum in nutrient-enriched sites and their "controls". (One sided t-tests, * = difference significant at p < 0.005). Character

nests

No. of plants Height (cm) Dry mass (g/plant) Heads/plant Head diameter Achenes/plant Achenes/head Achenes/cm 2 receptacle

25 162.2*

± 32.1

nests' control

waste places

waste control

13 70.4*

23 179.6*

25 53.9*

± 13.1

7.4 9.4 ± 6.4 5.1* ± 0.5 1727 194.9* ± 38.6

3.6 1 1.9* ± 0.7 41 40.7* ± 19.8

12.2

6.8

6.8 10.4*

± 31.9

2.3 1.2*

± 7.3

± 12.4

± 0.4

Table 4. Number of species, biomass and diversity in nutrient-enriched sites vs. their "controls". (One-sided t-tests, difference significant at * = p < 0.01 ** = p < 0.005 *** = p < 0.0005). Nests mean Species number /0.25 m 2 Biomass g/0.25 m 2 eH 204

S.D.

5.0***

Nests control

Waste

mean

mean

S.D.

1.2

20.4*** 5.0

974.4* 597.5 1.4** 0.6

155.8* 10.4 6.8** 3.0

FLORA (1994) 189

4.0***

Waste control S.D.

mean

S.D.

2.0

25.8*** 4.5

733.1 ** 339.1 1.1 ** 0.1

146.5** 20.1 9.8** 4.0

Table 5. Distribution rates of species according to their characteristic vegetation types in nutrient enriched habitats vs. their "controls", (X 2 test, *** = significant at p < 0.001). Vegetation type

percentage of species nests nests control

Synanthropic Herbaceous formation Mediterranean low shrub formation

6*** 92

waste waste control

25*** 6*** 94*** 75

50*** 50***

2

4. Discussion Silybum marianum is a ruderal myrmecochorous plant that dominates refuse zones of nests of Messor semirufus and waste places. We found that S. marianum in such habitats is "superior" in vegetative and reproductive traits (Table 3) to S. marianum individuals growing among the surrounding vegetation. At these specific sites, species diversity is considerably lower, whereas biomass is significantly higher (about 90% of which is of S. marianum biomass) than in control plots (Table 4). Our studies within the nests' area showed that in the plots where S. marianum had been harvested the number of species (and to some extent species diversity) increased (Table 1). Total biomass was significantly higher in the treated plots, indicating that the companion species, which otherwise were suppressed in the presence of S. marianum, did grow successfully. Dry biomass of most the individual companion species increased by over 150% in the treated plots (Table 2). These results point to the possibility that S. marianum has a competitively suppressive effect upon its companion species, other than Avena and Hordeum. Mean biomass values of the dominant grasses (present in over 50% of the treated plots) did not differ significantly from their mean values in the control plots. As tested by number of spikelets of A. slerilis, there was no evidence for higher fruit set in plots where S. marianum was removed. It could be inferred from these latter results that S. marianum does not affect A. slerilis, A. barbala and H. sponlaneum which presumably are adapted to grow in similar habitats. We found no experimental evidence for effective allelopathic influence of S. marianum on the germination of other species. Thus, its dominance in the nests is probably not due to allelopathy but rather to other adaptive traits advantageous in competition, such as fast growth and a rapid gain of biomass, as observed in this study. Large and aggressive plants are known to

utilize light and/or water resources with greater efficiency by which they may gain a higher population density (DAUBENMIRE 1974; HARPER 1977). "Changes in the population density of one plant species are likely to affect the avaliabilities of various resources, such as nitrogen, water, phosphorus and light, and thus influence the growth of other species indirectly" (TILMAN 1986). In consequence, the companion species would ultimately degenerate. Removal of the elaiosome (by ants or artificially) does not affect germinability. A high proportion (35% out of 10 species) of the seedlings around the nest are of S. marianum. Probably, a large seed bank around the nest, as well as in waste places, is formed by the highly fertile plants that grow there, contributing multitudes of seeds every season. Prevalence of S. marianum may be enhanced by myrmecochory, by which the number of S. marianum seeds in the seed bank is directly increased. In summation, the success of S. marianum in its particular habitats, whether primary (like the harvesting ants' nests) or secondary (like waste places), can be attributed to the vegetative and developmental qualities of the plant during its establishment and growth phases, culminating in high fecundity rates. These traits, now under further investigation, enable the plant to dominate its particular habitats at the expense of other plants. Both ants' nests and waste places are characterized by high percentages of synanthropic plants, as compared with the neighboring vegetation (Table 5). Before secondary habitats, like waste places, have been created by humans, the nitrophilous vegetation occurred on sites rich with organic matter, such as animals' resting places (ZOHARY 1973; PIGNATTI 1983). We assume that certain pre-adapted plants like S. marianum could immigrate into man-made habitats from ants' nests that seemingly were their primary habitats in the Mediterranean region.

5. References ALAVI, S. A. (1983): Silybum. In: JAFRI, S. M. H. & ELGADI, A. (eds.): Flora of Libya. Vol. 107. AI-Faateh University, Faculty of Science, Department of Botany, Tripoli. AVIDov, z. (1968): Harvester ants in Israel. Sifriath Hassadeh, Tel-Aviv (Hebrew). BEATTIE, A. J., & CULVER, D. C. (1981): The guild of Myrmecochores in the herbaceous flora of West Virginia forests. Ecology 62: 107 -115. BERG R. Y. (1975): Myrmecochorous plants in Australia and their dispersal by ants. Austral. J. Bot. 23: 475508. FLORA (1994) 189

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DANIN A., & YOM-TOY, Y. (1990): Ant nests as primary habitats of Silybum marianum (Compositae). Plant Syst. Evol. 169: 209-217. DATTA, S. C., & CHATTERJEE, A. K. (1980): Alle10pathic potential of Polygonum orientale L. in relation to germination and seedling growth of weeds. Flora 169: 456-465. DAUBENMIRE, R. F. (1974): Plants and environment. John Wiley and sons, London. DAVIDSON, D. w., & MORTON, S. R. (1981): Myrmecochory in some plants (F. Chenopodiaceae) of the Australian arid zone. Oecologia 50: 357 - 366. FEINBRUN-DoTHAN, N. (1978): Silybum ADANS. In: FEINBRUN-DoTHAN, N. Flora Palaestina. Part 3. The Israel Academy of Sciences and Humanities, Jerusalem. - & DANIN, A. (1991): Analytical flora of Eretz-Israel. Cana, Publishing House Ltd., Jerusalem (Hebrew). FRANCO, J. A. (1976): Silybum ADANSON. In: 1bTIN, T. G. et al. (eds.): Flora Europaea. Vol 4. Cambridge U niversity Press, Cambridge. FRIEDMAN, J., ORSHAN, G., & ZIGER-CFIR, Y. (1977): Suppression of annuals by Artemisia herba-alba in the Negev Desert ofIsrae1. J. Ecol. 65: 413-426. GENTRY, J. B., & STIRITZ, K. L. (1972): The role of the Florida harvester ant, Pogonomyrmex badius, in old field mineral nutrient relationships. Environm. Entomol. 1: 39-41. GLINSKI, J., & STEPNIEWSKI, W. (1985): Soil aeration and its role for plants. CRC Press, Boca Raton, Florida. HANDEL, S. N. (1978): The competitive relationship of three woodland sedges and its bearing on the evolution of ant dispersal of Carex pedunculata. Evolution 32: 151-163. HARPER, J. L. (1977): Population biology of plants. Academic Press, London.

206

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HILL, M. O. (1973): Diversity and evenness: a unifying notation and its consequences. Ecology 54: 427 -432. KUPICHA, F. K. (1975): Silybum ADANS. In: DAVIS, P. H. (ed.): Flora of Turkey and the East Aegean Islands. Vol. 5. Edinburgh. MULLER, C. H. (1966): The role of chemical inhibition (allelopathy) in vegetational composition. Bull. Torrey Bot. Club 93: 332-351. OFFER, J. (1980): The ecology of ant populations of the genus Messor and their influence on the soil and flora in pasture. Ph. D. thesis, The Hebrew University, Jerusalem (Hebrew). PEAKALL, R., OLIVER, I., ThRNBALL, C. L., & BEATTIE, A. J. (1993): Genetic diversity in an ant-dispersed Chenopod Sclerolaena diacantha. Austral. J. Ecol. 18: 171-179. PIGNATTI, S. (1983): Human impact on vegetation of the Mediterranean basin. In: HOLZNER, W., WERGER, M. J. A., & IKUSIMA, I. (eds.): Man's impact on vegetation. Dr. W. Junk Publishers, The Hague, Boston, London. RICE, B., & WESTOBY, M. (1981): Myrmecochory in sc1erophyll vegetation of the West-Head, New-South Wales. Austral. J. Bot. 6: 291-298. RICE, E. L. (1984): Allelopathy. 2nd edition, Academic Press, Orlando, Florida. TILMAN, D. (1986): Resources, competition and the dynamics of plant communities. In: CRAWLEY, M. J. (ed.): Plant ecology. Blackwell Scientific Publications. WESTOBY, M., FRENCH, K., HUGHES, L., RICE, B., & RODGERSON, L. (1991): Why do more plant species use ants for dispersal on infertile compared with fertile soils? Austral. J. Ecol. 16: 445-455. ZOHARY, M. (1973): Geobotanica1 foundations of the Middle East. Gustav Fischer, Stuttgart.