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Comparative analysis of variables associated with germination and seedling establishment for Prosopis nigra (Griseb.) Hieron and Acacia caven (Mol.) Mol.
Forest Ecology and Management 179 (2003) 15–25
Comparative analysis of variables associated with germination and seedling establishment for Prosopis nigra (Griseb.) Hieron and Acacia caven (Mol.) Mol. Paula Pratolongo*, Rube´n Quintana, Ine´s Malva´rez, Marcela Cagnoni Facultad de Ciencias Exactas y Naturales, Laboratorio de Ecologı´a Regional, Universidad de Buenos Aires, Ciudad Universitaria, Pabello´n 2, Piso 4, C1428EHA Buenos Aires, Argentina Received 12 September 2001; received in revised form 31 May 2002; accepted 16 June 2002
Abstract The purpose of this work was to compare different variables associated with the germination and growth of Prosopis nigra and Acacia caven seedlings. Fieldwork was carried out in 1999 on materials collected in Entre Rı´os province, Argentina. Germination percentages and rates were measured in order to determine the effect of immersion in water for different periods of time and of the ingestion of P. nigra fruits by the greater rhea. Seedling growth was compared for both species as a function of stem elongation, increase in volume, leaf production rate and survival percentage during the first 60 days following germination. Results indicate that, unlike A. caven, P. nigra seeds are negatively affected by immersion in water as seeds submitted to different immersion periods showed a significant decrease in final germination percentages with respect to untreated seeds. P. nigra seeds ingested by the greater rhea also showed lower final germination percentages as compared to those not ingested. Nevertheless, those that succeeded in germinating achieved significantly higher germination velocities. A. caven seedlings attained significantly higher heights than those of P. nigra from the 20th day onwards. Volume growth for A. caven was also higher, as well as leaf production and survival until the 60th day. Results suggests that in order to maintain P. nigra dominance, practices favoring prolonged waterlogging periods should be avoided, thus promoting a high seedling yield. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Argentina; Parana´ River Delta; Germination; Seedling growth; Seedling survival; Acacia caven; Prosopis nigra
1. Introduction The effects of land use on the dynamics of plant communities in different ecosystems are substantial for plant ecology (Acher, 1990). Such effects have been widely studied in the case of communities dominated by different species of the Prosopis genus on *
Corresponding author. Tel.: þ54-11-4576-3300-212; fax: þ54-11-4576-3384. E-mail address: [email protected] (P. Pratolongo).
account of their economic significance for local population (Morello et al., 1985; Acher, 1990, 1995; Ada´moli et al., 1990; Scanlan and Acher, 1991; East and Felker, 1993). In southern Entre Rı´os (Argentina), included in the Parana´ River Delta region, there is an extended area alternatively subjected to temporary waterlogging and drought, a regime determined by particular topographic and edaphic characteristics (Malva´rez, 1997). In some communities of the area, the woody layer is dominated by Prosopis nigra. Historically, these
0378-1127/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 2 ) 0 0 5 4 5 - 5
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environments have been subjected to intense selective logging and grazing which dramatically modified the original specific composition in areas of high disruption intensity. Acacia caven is the dominant woody species in such disturbed locations (Pratolongo, 2000). The stages of germination and seedling establishment are critical in the life history of woody plants and condition their density as well as specific community composition (Grubb, 1977). Thus, any disturbance affecting these stages also affects the future composition of such communities. Variations in hydrological regime (Gosselink and Turner, 1978; Neiff, 1990; Brinson, 1993; Mitsch and Gosselink, 1993) and the presence of frugivorous animals (Mooney et al., 1977; Traveset, 1998) affect seed germination. Besides, each species initial growth rate strongly affects, and even determines, seedling establishment (Drury and Nisbet, 1973; Connell and Slatyer, 1977; Huston and Smith, 1987). In this region, the hydrological regime may also be affected by soils highly liable to compaction (Bonfils, 1962; Go´ mez and Ferrao, 1986; Malva´ rez, 1997; Baumann, 1999; Pratolongo, 2000) and by cattle raising, since cattle trampling reduces pore space and soil infiltration capacity, extending waterlogging periods after precipitation. Greater rhea (Rhea americana) is usual in this region. The share of P. nigra fruits in this animal’s diet is very high (Pereira, 2002) and might influence various aspects related to seed germination (Traveset, 1998). Moreover, studies carried out on different species of Prosopis indicate that, in humid climates, competition is a decisive factor for a successful seedling establishment (Villagra, 2000; Passera, 2000). In this case, competition might be embodied in the competitive relationships between P. nigra and A. caven. Generally, rapid growth is considered as highly advantageous since it favors resource appropriation by seedlings and therefore increases successful establishment probabilities (Mooney et al., 1977). The present work was directed first at determining how temporary waterlogging and the frugivorous habits of the greater rhea affect A. caven and P. nigra seed germinating power. Second, it was directed at comparing seedling growth in both species during the first 60 days following germination in order to infer eventual competitive advantages at this stage.
2. Materials and methods 2.1. Study area The study area is located at ‘‘Don Jose´ ’’ ranch (338270 S, 588480 W), 6 km due north of Ceibas, Department of Gualeguaychu´ , Entre Rı´os province, Argentina. It is included in one of the 11 wetland landscape units already identified for the Delta of Parana´ River region (Fig. 1). The landscape pattern corresponds to plains with a savanna physiognomy of grasses and patches of xerophytic P. nigra and A. caven forests and baldspots, sites with a large percentage of bare soil and little cover of Portulaca sp. The area is also crisscrossed by small lentic streams covered with aquatic plants (Malva´ rez, 1997). Mean annual rainfall is 978 mm, and temperature averages 17.4 8C. Unlike neighboring areas, it is free of the periodical floods of the Parana´ River. Although it only gets rainfall water, large waterlogged tracts due to the minimum slope of the land (Malva´ rez, 1997) and the type of soils may also be observed (Pratolongo, 2000).
Fig. 1. Geographical location of the Parana´ River Delta Region. The landscape unit in which the study was carried out is shown in gray.
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The soil profile in more elevated lots, which are home to woody vegetation, shows a shallow clayey horizon with high sodium content (Baumann, 1999). This is fundamental for surface water dynamics, since sodium operates as a clay-dispersing agent that promotes clay expansion in contact with water and generates a virtually impermeable layer responsible for waterlogging above this level (Buol et al., 1991; Duchaufour, 1975). The specific geomorphologic and edaphic conditions of this landscape unit result in low agricultural yields. Hence, extensive cattle breeding is the main economic activity. Besides, local settlers carry out intense wildlife extraction activities, especially timber from P. nigra, which is used both as a fuel and in fence post-manufacturing. 2.2. Germination Seeds and greater rhea faeces used for germination were collected during the month of March, 1999. Both faeces and whole fruits were stored in well-aerated wooden boxes at room temperature and protected from rain. In May 1999, the first germination was completed in order to determine germination percentages and rates for each type of seed. Thus, 495 seeds of A. caven, 110 seeds of P. nigra, and 139 seeds of P. nigra from greater rhea faeces were used. In September 1999, a second germination was completed, which included water-immersion pregermination treatments applied to the three seed types (A. caven, P. nigra and P. nigra from rhea faeces). Three different treatments were applied: no immersion, 7 days, and 14 days immersion periods. Eleven repetitions were used for each combination of seed type and treatment, with 50 seeds for each repetition. Both germinations were conducted in darkness at room temperature by placing seeds on a filter paper whose dampness was maintained throughout the experience. In the case of A. caven, hulled seeds were used since open fruits and scattered seeds are not unusual out in the open. In the case of P. nigra, whose fruits come off the plant as a simple, indehiscent structure (Mooney et al., 1977), covered endocarp segments were directly used so as to enable comparison with naked segments from greater rhea faeces since, upon passing through the digestive tract, pulp is separated from the endocarp. For each tray, the number of germinated
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seeds was recorded daily. In every case, germination was defined as the moment when the radicle emerged (ISTA, 1985). Accumulated germination data over time were fitted to a logistic function ðf ðxÞ ¼ b=ð1 þ eagx ÞÞ. This function was selected because it yields patterns that closely resemble those of germination curves for slow germinating seed samples (Hartmann and Kester, 1980). In order to study the effect of previous immersion on A. caven and non-ingested P. nigra seeds, a two-way ANOVA test and Tukey’s multiple comparisons were conducted using final germination percentages recorded in September. The effect of the three previous treatments on seeds ingested by R. americana were also analyzed by applying a one-way Kruskal– Wallis test and Dunn’s multiple comparisons. The effect of ingestion on the final germination percentage of untreated P. nigra seeds was assessed through a one-way ANOVA test. Differences in germination rates were analyzed through a one-way Kruskal–Wallis test. Finally, the sustainability of germination ability over time was examined through three Gauss tests (Steel and Torrie, 1985) in order to compare the final germination percentages in May and September for each of the three types of seeds being considered. 2.3. Seedling growth The growth of each seedling was followed individually, considering time of radicle emergence as the day of germination. Each germinated seed was assigned to a numbered plastic container previously filled with a mixture of silt loam soil, sand, and organic sediments (2:1:1). Cultures were maintained at room temperature with the substrate permanently damp. Stem height, stem diameter at the crown, and the number of leaves were recorded for each seedling. Initial data were recorded at the 10th day after radicle emergence and later repeated for every 10 days during the 60 days period. In order to study stem height increase through time, an ANOVA test with a repeated measures design was conducted. The lower-bound Epsilon adjustment was used since it provides the most conservative approximation (Greenhouse and Geisser, 1959; Potvin and Lechowicz, 1990). The stem volume was computed for each seedling as a function of its length (L) and the crown diameter
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(f), according to the following function: V ¼ pðf=2Þ2 L. For each time period starting from radicle emergence (T) onwards, the volume change rate was computed as V/T. In order to determine if volume change rate was constant over time, stem volume was fitted to a linear function of time. Once the rate was determined to be constant throughout the 60 days involved in the experience, the mean rate over the six measurements was calculated for each seedling. A one-way ANOVA test was then carried out on the resulting variable in order to determine differences between the two species. Similarly, the leaf production rate was estimated as number of leaves/time (T). As in the previous case, the variable tested was the mean rate for each seedling, after fitting the number of leaves to a linear function of time and verifying that the rate was constant throughout the period in question. The percentage of surviving seedlings was assessed by comparing the number of individuals that survived until the 60th day (S) with the total number of germinated seeds (G). Survival percentages for both species were analyzed through a Gauss test for percentage samples (Steel and Torrie, 1985).
3. Results 3.1. Germination P. nigra seeds that were not submerged reached higher germination percentages than those of A. caven (Fig. 2). Seeds of P. nigra subjected to previous immersion showed lower germination percentages than non-immersed seeds, while seeds of A. caven were apparently not affected by these treatments. The results of the two-way ANOVA and Tukey’s tests
shown in Table 1 indicate that non-immersed P. nigra seeds reached germination percentages significantly higher (P < 0:01) than those of A. caven whereas, in the case of submerged seeds, the differences between the two species were negligible. The comparison of germination percentages in ingested seeds of P. nigra yielded the following results: the response was similar to that of non-ingested seeds subjected to the same treatments of immersion (Fig. 3). Submerged seeds showed a significant reduction in germination percentage as compared to non-treated seeds (Kruskal– Wallis test, H ¼ 24:44; n ¼ 11; P < 0:01) and significant differences were evident between each couple of treatments (Dunn’s multiple comparisons test; P < 0:05). Seed passage through the digestive tract of the greater rhea affected both the final percentage and the germination rate (Fig. 4). Non-ingested seeds reached final percentages significantly higher than those taken from faeces (mean standard deviation values being 10:91 4:50 and 32:00 9:96% for ingested and non-ingested seeds, respectively; P < 0:01). Ingested seeds attained final germination percentage sooner. The time elapsed until germination in the case of ingested seeds was significantly shorter than the one required for non-ingested seeds. Median values were 4 and 17 days, respectively (Kruskal– Wallis test, H ¼ 69:43; P < 0:01). Ingested seeds also showed a smaller dispersion around the median, so that most of them germinated in a very narrow time range (Fig. 5). Neither A. caven seeds nor those of P. nigra extracted from greater rhea faeces showed significant differences in germination percentage in September as compared to the corresponding values in May. On the other hand, non-ingested P. nigra seeds showed a significantly lower germination percentage in September (Table 2).
Table 1 Final germination percentages for each combination of species and germination pretreatmenta Species
P. nigra A. caven
Final germination percentage (%) 14 days immersion
7 days immersion
No immersion
5.82 6.54 a 10.55 3.91 b
6.91 3.02 d 4.91 2.59 c
32.00 9.96 abcde 9.37 7.42 e
a Values indicate the mean standard deviation for 11 repetitions. The same letters between each couple of treatments indicate significant differences at P < 0:01 (Tukey’s test).
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Fig. 2. Cumulative germination percentages for A. caven and P. nigra seeds submitted to different germination pretreatments: (~) 14 days of previous immersion in water; (&) 7 days of previous immersion; (*) no immersion. Values obtained in September were fitted to logistic functions (R2 > 90%).
3.2. Seedling growth From the 20th day after the radicle emerged until the end of the experience, A. caven seedlings showed a
mean height superior to that of P. nigra (Fig. 6). When the assumptions of the ANOVA test were discussed, it was accepted that data were well fitted to a normal distribution (Lilliefors normality test; P > 0:01) and
Table 2 Final germination percentages for May and September
A. caven seeds Non-ingested P. nigra seeds P. nigra seeds ingested by greater rhea *
Significant differences (P < 0:01).
May (%)
September (%)
6.88 55.45 9.35
9.64 32.00 10.91
Gauss’s statistics (e) 1.63 4.56* 0.56
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Fig. 3. Cumulative germination percentages for P. nigra seeds from greater rhea faeces: (~) 14 days of previous immersion in water; (&) 7 days of previous immersion; (*) no immersion. Values obtained in September were fitted to logistic functions (R2 > 0:90).
that the variance/covariance matrices were homogeneous (Box M ¼ 33:39; P > 0:06). However, the compound symmetry assumption was rejected (Mauchley’s sphericity test; P < 0:01). Hence, the lower-bound Epsilon adjustment was selected because it provides a widely used approximation to compensate for the violation of this assumption. According to the ANOVA test results, the hypothesis of parallelism was rejected (n ¼ 59; P < 0:01).
No significant difference between the two species is evident until the 10th day after germination. However, from the 20th day onwards, A. caven seedlings are significantly higher than those of P. nigra, and the difference increases with time (Table 3). Stem volume and number of leaves were both well fitted to linear functions of time (Table 4). Thus, volume change and leaf production rates were both considered constant during the 60 days period. When
Fig. 4. Cumulative germination percentages for non-pretreated P. nigra seeds: (&) seeds from greater rhea faeces; (~) non-ingested seeds. Values obtained in September were fitted to logistic functions (R2 > 0:90).
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Table 4 Coefficient of determination (R2) obtained for the linear regressions of stem volume and number of leaves (dependent variables) vs time (independent variable) for both tree speciesa Coefficient of determination (R2)
P. nigra A. caven
Volume of stem
Number of leaves
0.65 0.99
0.99 0.98
a The coefficient indicates the proportion of variance accounted for the dependent variable by the linear model.
Fig. 5. Number of days elapsed until germination for ingested and non-ingested P. nigra seeds: (&) median; (&) 25–75%; ( ) minimum and maximum values.
comparing volume change rate in the two species under study (Fig. 7), A. caven seedlings showed higher rates (2:40 1:42 mm3 per day vs 0:76 0:54 mm3 per day, mean standard deviation for A. caven and P. nigra, respectively; n ¼ 59; P < 0:01).
A. caven seedlings have shown higher number of leaves through the time considered (Fig. 8). The ANOVA test indicated that leaf production rate was significantly higher for A. caven seedlings (0:05 0:04 and 0:16 0:06 leaves per day for P. nigra and A. caven, respectively; P < 0:01). Final survival percentages also showed significant differences. Nearly all germinated A. caven seeds survived at least 50 days and the final survival percentage
Fig. 6. Mean values for stem height (mm) of P. nigra (~) and A. caven (&) seedlings (n ¼ 59). Table 3 Mean standard deviation values for stem height (mm) of P. nigra and A. caven seedlings (n ¼ 59) Stem height (mm) 10 days P. nigra A. caven P *
13.20 3.57 13.08 3.85 >0.7
20 days
30 days
40 days
50 days
60 days
16.43 3.34 19.67 4.76 <0.01*
26.92 8.06 31.46 8.97 <0.01*
36.41 10.76 46.07 11.58 <0.01*
46.71 14.07 60.28 15.54 <0.01*
59.51 18.11 80.27 22.11 <0.01*
Significant differences between species.
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Fig. 7. Volume of stems (mean values corresponds to seedlings that survived until the 60th day). Values for P. nigra (~) and A. caven (&) were fitted to lineal functions.
Fig. 8. Mean number of leaves. Values for P. nigra (~) and A. caven (&) were fitted to linear functions.
of A. caven seedlings was significantly higher than the corresponding figure for P. nigra (86.77 and 67.24%, respectively; Gauss test e ¼ 3:26; P < 0:01).
4. Discussion P. nigra seeds were adversely affected by waterimmersion, indicating perhaps that an increase in
waterlogging periods might affect new recruits of P. nigra thus altering the dominance pattern of this community woody layer. Because of the edaphic conditions of the area, surface horizon compaction due to cattle trampling might have a crucial influence on the soil water retention capacity because of the low permeability in the underlying horizon. An exceedingly high compaction might entail a change in soil response to equally intense
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precipitation, generating thus long waterlogging periods and, consequently, negative effects on P. nigra seed germination. The results obtained in this study suggest that a high animal load might have a differential effect on regeneration for the two species involved, since waterlogging due to cattle trampling might have dangerous effects for P. nigra germination and minimal effects on A. caven. Although P. nigra fruit ingestion by the greater rhea negatively affected final germination percentages, it also decreased the time required for germination. This may be due to digestion damage on the endocarp cover, a process that exposes the seed and favors water absorption once faeces are eliminated. Therefore, surviving seeds might germinate sooner and it might constitute an escape strategy against rodent and insect predation. Thus, the role of the greater rhea in this species regeneration might be substantial, since seed predation has been indicated as a decisive factor on the population dynamics of the Prosopis genus (Solbrig and Cantino, 1975; Villagra, 2000). Besides, fruit ingestion might keep up seed germination capability over longer periods of time. It has been remarked that P. nigra seeds are attacked by various internal parasites, especially insect larvae of the Bruchidae family, such as Rhipibruchus picturatus Fahr., R. prosopis King., and at least three different species of the Scutobruchus genus (Kingsolver et al., 1977). According to some authors (Janzen, 1969; Hauser, 1994; Miller, 1996), the digestive fluids of frugivorous animals might be lethal for parasite larvae, thus preventing the development of adult insects that lay eggs on healthy seeds. However, since this process has not been proven yet for P. nigra seeds ingested by the greater rhea, no detailed analysis of the mechanism involved in germinating power preservation through this frugivorous animal is provided. Studies on different species of the Prosopis genus indicate that their growth is extremely slow during the earlier stages of development (Catala´ n et al., 1994; Orfila, 1995; Felker, 1996) and that, under natural conditions, seedlings show very low survival percentages (Scifres and Brock, 1970a, 1970b). In this study, P. nigra seedling survival was low, even for experimental conditions, and even lower figures can be expected under natural conditions where hydric stress and the herbivorous habits of neighboring
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animals are important mortality factors. Considering the high mortality rate, it might be assumed that a high number of recruits depends to a great extent on the successful germination of a similarly great number of seeds. Thus, unfavorable conditions for germination might implies that no seed produced in a certain year develops into a recruit. A. caven seedlings quickly develop a stronger structure that results in higher survival percentages. When compared to P. nigra seedlings, those of A. caven show some characteristics that may involve significant competitive advantages for establishment, such as a swift stem elongation and a high leaf production rate. Thus, A. caven seeds that succeed in germinating may have a higher probability of generating recruits.
5. Conclusion Various studies have shown the importance of different Prosopis species in ecosystems because they generate specific conditions that favor associated animal populations and plant communities (Kingsolver et al., 1977; Mares et al., 1977). These evidences suggest that P. nigra woods in the study area play a significant role in maintaining the structure and working order of the landscape by creating patches of specific physiognomy and composition, which constitute an habitat and food source for many wildlife species. This landscape may be preserved throughout time by taking into account the early development stage characteristics of P. nigra, the dominant species in slightly disturbed areas, and also of A. caven, the most favored species in highly disrupted areas. According to the results herein discussed, maintaining favorable conditions for P. nigra germination seems crucial for regenerating this species. Moreover, overgrazing appears as a decisive factor, not only because of its direct consequences on seedling and recruit consumption, but also because it highly modifies the soil permeability.
Acknowledgements We wish to thank Mr. I. Schojett for allowing the study to be conducted on his ranch, and S. Arias, J. Pereira, V. Cirelli, N. Fracassi, M. Biondini and M.
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Srur for their field support. A special thanks to the anonymous reviewers for constructive criticism. This research was carried forth through the TX-16 grant of the UBACyT Program of the Buenos Aires University and PICT 98 no. 04503 grant of the FONCYT Program of the Agencia de Promocio´ n Cientı´fica y Tecnolo´ gica.
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P. Pratolongo et al. / Forest Ecology and Management 179 (2003) 15–25 Pratolongo, P., 2000. Ana´ lisis estructural de poblaciones de Prosopis nigra (Griseb.) Hieron y Acacia caven (Mol.) Mol. del sur de Entre Rı´os y comparacio´ n experimental de variables ligadas a la germinacio´ n y el crecimiento de las pla´ ntulas. Tesis de Licenciatura. Universidad de Buenos Aires, Buenos Aires. Scanlan, J.C., Acher, S., 1991. Simulated dynamics of succession in a North American subtropical Prosopis savanna. J. Veg. Sci. 2, 625–634. Scifres, C.J., Brock, J.H., 1970a. Moisture–temperature interrelations in germination and early seedling development of honey mesquite. Texas Agr. Expt. Sta. Texas A&M University, P.R.2816. Scifres, C.J., Brock, J.H., 1970b. Growth and development of honey mesquite seedlings in the field and greenhouse as related
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to time of planting, planting depth, soil temperature and top removal. Texas Agr. Expt. Sta. Texas A&M University, P.R.2817. Solbrig, O.T., Cantino, P.D., 1975. Reproductive adaptations in Prosopis (Leguminosae, Mimosoideae). J. Arnold Arboretum 56, 185–210. Steel, R.G.D., Torrie, J.H., 1985. Bio estadı´stica. Principios y procedimientos. McGraw-Hill, Bogota´ . Traveset, A., 1998. Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect. Plant Ecol. Evol. Syst. 1, 151–190. Villagra, P.E., 2000. Aspectos ecolo´ gicos de los algarrobales argentinos. Libro de resu´ menes. Reunio´ n Nacional del Agarrobo. III. Reunio´ n de la Asociacio´ n Argentina de Prosopis, Mendoza.
Comparative analysis of variables associated with germination and seedling establishment for Prosopis nigra (Griseb.) Hieron and Acacia caven (Mol.) Mol. Paula Pratolongo*, Rube´n Quintana, Ine´s Malva´rez, Marcela Cagnoni Facultad de Ciencias Exactas y Naturales, Laboratorio de Ecologı´a Regional, Universidad de Buenos Aires, Ciudad Universitaria, Pabello´n 2, Piso 4, C1428EHA Buenos Aires, Argentina Received 12 September 2001; received in revised form 31 May 2002; accepted 16 June 2002
Abstract The purpose of this work was to compare different variables associated with the germination and growth of Prosopis nigra and Acacia caven seedlings. Fieldwork was carried out in 1999 on materials collected in Entre Rı´os province, Argentina. Germination percentages and rates were measured in order to determine the effect of immersion in water for different periods of time and of the ingestion of P. nigra fruits by the greater rhea. Seedling growth was compared for both species as a function of stem elongation, increase in volume, leaf production rate and survival percentage during the first 60 days following germination. Results indicate that, unlike A. caven, P. nigra seeds are negatively affected by immersion in water as seeds submitted to different immersion periods showed a significant decrease in final germination percentages with respect to untreated seeds. P. nigra seeds ingested by the greater rhea also showed lower final germination percentages as compared to those not ingested. Nevertheless, those that succeeded in germinating achieved significantly higher germination velocities. A. caven seedlings attained significantly higher heights than those of P. nigra from the 20th day onwards. Volume growth for A. caven was also higher, as well as leaf production and survival until the 60th day. Results suggests that in order to maintain P. nigra dominance, practices favoring prolonged waterlogging periods should be avoided, thus promoting a high seedling yield. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Argentina; Parana´ River Delta; Germination; Seedling growth; Seedling survival; Acacia caven; Prosopis nigra
1. Introduction The effects of land use on the dynamics of plant communities in different ecosystems are substantial for plant ecology (Acher, 1990). Such effects have been widely studied in the case of communities dominated by different species of the Prosopis genus on *
Corresponding author. Tel.: þ54-11-4576-3300-212; fax: þ54-11-4576-3384. E-mail address: [email protected] (P. Pratolongo).
account of their economic significance for local population (Morello et al., 1985; Acher, 1990, 1995; Ada´moli et al., 1990; Scanlan and Acher, 1991; East and Felker, 1993). In southern Entre Rı´os (Argentina), included in the Parana´ River Delta region, there is an extended area alternatively subjected to temporary waterlogging and drought, a regime determined by particular topographic and edaphic characteristics (Malva´rez, 1997). In some communities of the area, the woody layer is dominated by Prosopis nigra. Historically, these
0378-1127/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 2 ) 0 0 5 4 5 - 5
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environments have been subjected to intense selective logging and grazing which dramatically modified the original specific composition in areas of high disruption intensity. Acacia caven is the dominant woody species in such disturbed locations (Pratolongo, 2000). The stages of germination and seedling establishment are critical in the life history of woody plants and condition their density as well as specific community composition (Grubb, 1977). Thus, any disturbance affecting these stages also affects the future composition of such communities. Variations in hydrological regime (Gosselink and Turner, 1978; Neiff, 1990; Brinson, 1993; Mitsch and Gosselink, 1993) and the presence of frugivorous animals (Mooney et al., 1977; Traveset, 1998) affect seed germination. Besides, each species initial growth rate strongly affects, and even determines, seedling establishment (Drury and Nisbet, 1973; Connell and Slatyer, 1977; Huston and Smith, 1987). In this region, the hydrological regime may also be affected by soils highly liable to compaction (Bonfils, 1962; Go´ mez and Ferrao, 1986; Malva´ rez, 1997; Baumann, 1999; Pratolongo, 2000) and by cattle raising, since cattle trampling reduces pore space and soil infiltration capacity, extending waterlogging periods after precipitation. Greater rhea (Rhea americana) is usual in this region. The share of P. nigra fruits in this animal’s diet is very high (Pereira, 2002) and might influence various aspects related to seed germination (Traveset, 1998). Moreover, studies carried out on different species of Prosopis indicate that, in humid climates, competition is a decisive factor for a successful seedling establishment (Villagra, 2000; Passera, 2000). In this case, competition might be embodied in the competitive relationships between P. nigra and A. caven. Generally, rapid growth is considered as highly advantageous since it favors resource appropriation by seedlings and therefore increases successful establishment probabilities (Mooney et al., 1977). The present work was directed first at determining how temporary waterlogging and the frugivorous habits of the greater rhea affect A. caven and P. nigra seed germinating power. Second, it was directed at comparing seedling growth in both species during the first 60 days following germination in order to infer eventual competitive advantages at this stage.
2. Materials and methods 2.1. Study area The study area is located at ‘‘Don Jose´ ’’ ranch (338270 S, 588480 W), 6 km due north of Ceibas, Department of Gualeguaychu´ , Entre Rı´os province, Argentina. It is included in one of the 11 wetland landscape units already identified for the Delta of Parana´ River region (Fig. 1). The landscape pattern corresponds to plains with a savanna physiognomy of grasses and patches of xerophytic P. nigra and A. caven forests and baldspots, sites with a large percentage of bare soil and little cover of Portulaca sp. The area is also crisscrossed by small lentic streams covered with aquatic plants (Malva´ rez, 1997). Mean annual rainfall is 978 mm, and temperature averages 17.4 8C. Unlike neighboring areas, it is free of the periodical floods of the Parana´ River. Although it only gets rainfall water, large waterlogged tracts due to the minimum slope of the land (Malva´ rez, 1997) and the type of soils may also be observed (Pratolongo, 2000).
Fig. 1. Geographical location of the Parana´ River Delta Region. The landscape unit in which the study was carried out is shown in gray.
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The soil profile in more elevated lots, which are home to woody vegetation, shows a shallow clayey horizon with high sodium content (Baumann, 1999). This is fundamental for surface water dynamics, since sodium operates as a clay-dispersing agent that promotes clay expansion in contact with water and generates a virtually impermeable layer responsible for waterlogging above this level (Buol et al., 1991; Duchaufour, 1975). The specific geomorphologic and edaphic conditions of this landscape unit result in low agricultural yields. Hence, extensive cattle breeding is the main economic activity. Besides, local settlers carry out intense wildlife extraction activities, especially timber from P. nigra, which is used both as a fuel and in fence post-manufacturing. 2.2. Germination Seeds and greater rhea faeces used for germination were collected during the month of March, 1999. Both faeces and whole fruits were stored in well-aerated wooden boxes at room temperature and protected from rain. In May 1999, the first germination was completed in order to determine germination percentages and rates for each type of seed. Thus, 495 seeds of A. caven, 110 seeds of P. nigra, and 139 seeds of P. nigra from greater rhea faeces were used. In September 1999, a second germination was completed, which included water-immersion pregermination treatments applied to the three seed types (A. caven, P. nigra and P. nigra from rhea faeces). Three different treatments were applied: no immersion, 7 days, and 14 days immersion periods. Eleven repetitions were used for each combination of seed type and treatment, with 50 seeds for each repetition. Both germinations were conducted in darkness at room temperature by placing seeds on a filter paper whose dampness was maintained throughout the experience. In the case of A. caven, hulled seeds were used since open fruits and scattered seeds are not unusual out in the open. In the case of P. nigra, whose fruits come off the plant as a simple, indehiscent structure (Mooney et al., 1977), covered endocarp segments were directly used so as to enable comparison with naked segments from greater rhea faeces since, upon passing through the digestive tract, pulp is separated from the endocarp. For each tray, the number of germinated
17
seeds was recorded daily. In every case, germination was defined as the moment when the radicle emerged (ISTA, 1985). Accumulated germination data over time were fitted to a logistic function ðf ðxÞ ¼ b=ð1 þ eagx ÞÞ. This function was selected because it yields patterns that closely resemble those of germination curves for slow germinating seed samples (Hartmann and Kester, 1980). In order to study the effect of previous immersion on A. caven and non-ingested P. nigra seeds, a two-way ANOVA test and Tukey’s multiple comparisons were conducted using final germination percentages recorded in September. The effect of the three previous treatments on seeds ingested by R. americana were also analyzed by applying a one-way Kruskal– Wallis test and Dunn’s multiple comparisons. The effect of ingestion on the final germination percentage of untreated P. nigra seeds was assessed through a one-way ANOVA test. Differences in germination rates were analyzed through a one-way Kruskal–Wallis test. Finally, the sustainability of germination ability over time was examined through three Gauss tests (Steel and Torrie, 1985) in order to compare the final germination percentages in May and September for each of the three types of seeds being considered. 2.3. Seedling growth The growth of each seedling was followed individually, considering time of radicle emergence as the day of germination. Each germinated seed was assigned to a numbered plastic container previously filled with a mixture of silt loam soil, sand, and organic sediments (2:1:1). Cultures were maintained at room temperature with the substrate permanently damp. Stem height, stem diameter at the crown, and the number of leaves were recorded for each seedling. Initial data were recorded at the 10th day after radicle emergence and later repeated for every 10 days during the 60 days period. In order to study stem height increase through time, an ANOVA test with a repeated measures design was conducted. The lower-bound Epsilon adjustment was used since it provides the most conservative approximation (Greenhouse and Geisser, 1959; Potvin and Lechowicz, 1990). The stem volume was computed for each seedling as a function of its length (L) and the crown diameter
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(f), according to the following function: V ¼ pðf=2Þ2 L. For each time period starting from radicle emergence (T) onwards, the volume change rate was computed as V/T. In order to determine if volume change rate was constant over time, stem volume was fitted to a linear function of time. Once the rate was determined to be constant throughout the 60 days involved in the experience, the mean rate over the six measurements was calculated for each seedling. A one-way ANOVA test was then carried out on the resulting variable in order to determine differences between the two species. Similarly, the leaf production rate was estimated as number of leaves/time (T). As in the previous case, the variable tested was the mean rate for each seedling, after fitting the number of leaves to a linear function of time and verifying that the rate was constant throughout the period in question. The percentage of surviving seedlings was assessed by comparing the number of individuals that survived until the 60th day (S) with the total number of germinated seeds (G). Survival percentages for both species were analyzed through a Gauss test for percentage samples (Steel and Torrie, 1985).
3. Results 3.1. Germination P. nigra seeds that were not submerged reached higher germination percentages than those of A. caven (Fig. 2). Seeds of P. nigra subjected to previous immersion showed lower germination percentages than non-immersed seeds, while seeds of A. caven were apparently not affected by these treatments. The results of the two-way ANOVA and Tukey’s tests
shown in Table 1 indicate that non-immersed P. nigra seeds reached germination percentages significantly higher (P < 0:01) than those of A. caven whereas, in the case of submerged seeds, the differences between the two species were negligible. The comparison of germination percentages in ingested seeds of P. nigra yielded the following results: the response was similar to that of non-ingested seeds subjected to the same treatments of immersion (Fig. 3). Submerged seeds showed a significant reduction in germination percentage as compared to non-treated seeds (Kruskal– Wallis test, H ¼ 24:44; n ¼ 11; P < 0:01) and significant differences were evident between each couple of treatments (Dunn’s multiple comparisons test; P < 0:05). Seed passage through the digestive tract of the greater rhea affected both the final percentage and the germination rate (Fig. 4). Non-ingested seeds reached final percentages significantly higher than those taken from faeces (mean standard deviation values being 10:91 4:50 and 32:00 9:96% for ingested and non-ingested seeds, respectively; P < 0:01). Ingested seeds attained final germination percentage sooner. The time elapsed until germination in the case of ingested seeds was significantly shorter than the one required for non-ingested seeds. Median values were 4 and 17 days, respectively (Kruskal– Wallis test, H ¼ 69:43; P < 0:01). Ingested seeds also showed a smaller dispersion around the median, so that most of them germinated in a very narrow time range (Fig. 5). Neither A. caven seeds nor those of P. nigra extracted from greater rhea faeces showed significant differences in germination percentage in September as compared to the corresponding values in May. On the other hand, non-ingested P. nigra seeds showed a significantly lower germination percentage in September (Table 2).
Table 1 Final germination percentages for each combination of species and germination pretreatmenta Species
P. nigra A. caven
Final germination percentage (%) 14 days immersion
7 days immersion
No immersion
5.82 6.54 a 10.55 3.91 b
6.91 3.02 d 4.91 2.59 c
32.00 9.96 abcde 9.37 7.42 e
a Values indicate the mean standard deviation for 11 repetitions. The same letters between each couple of treatments indicate significant differences at P < 0:01 (Tukey’s test).
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Fig. 2. Cumulative germination percentages for A. caven and P. nigra seeds submitted to different germination pretreatments: (~) 14 days of previous immersion in water; (&) 7 days of previous immersion; (*) no immersion. Values obtained in September were fitted to logistic functions (R2 > 90%).
3.2. Seedling growth From the 20th day after the radicle emerged until the end of the experience, A. caven seedlings showed a
mean height superior to that of P. nigra (Fig. 6). When the assumptions of the ANOVA test were discussed, it was accepted that data were well fitted to a normal distribution (Lilliefors normality test; P > 0:01) and
Table 2 Final germination percentages for May and September
A. caven seeds Non-ingested P. nigra seeds P. nigra seeds ingested by greater rhea *
Significant differences (P < 0:01).
May (%)
September (%)
6.88 55.45 9.35
9.64 32.00 10.91
Gauss’s statistics (e) 1.63 4.56* 0.56
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Fig. 3. Cumulative germination percentages for P. nigra seeds from greater rhea faeces: (~) 14 days of previous immersion in water; (&) 7 days of previous immersion; (*) no immersion. Values obtained in September were fitted to logistic functions (R2 > 0:90).
that the variance/covariance matrices were homogeneous (Box M ¼ 33:39; P > 0:06). However, the compound symmetry assumption was rejected (Mauchley’s sphericity test; P < 0:01). Hence, the lower-bound Epsilon adjustment was selected because it provides a widely used approximation to compensate for the violation of this assumption. According to the ANOVA test results, the hypothesis of parallelism was rejected (n ¼ 59; P < 0:01).
No significant difference between the two species is evident until the 10th day after germination. However, from the 20th day onwards, A. caven seedlings are significantly higher than those of P. nigra, and the difference increases with time (Table 3). Stem volume and number of leaves were both well fitted to linear functions of time (Table 4). Thus, volume change and leaf production rates were both considered constant during the 60 days period. When
Fig. 4. Cumulative germination percentages for non-pretreated P. nigra seeds: (&) seeds from greater rhea faeces; (~) non-ingested seeds. Values obtained in September were fitted to logistic functions (R2 > 0:90).
P. Pratolongo et al. / Forest Ecology and Management 179 (2003) 15–25
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Table 4 Coefficient of determination (R2) obtained for the linear regressions of stem volume and number of leaves (dependent variables) vs time (independent variable) for both tree speciesa Coefficient of determination (R2)
P. nigra A. caven
Volume of stem
Number of leaves
0.65 0.99
0.99 0.98
a The coefficient indicates the proportion of variance accounted for the dependent variable by the linear model.
Fig. 5. Number of days elapsed until germination for ingested and non-ingested P. nigra seeds: (&) median; (&) 25–75%; ( ) minimum and maximum values.
comparing volume change rate in the two species under study (Fig. 7), A. caven seedlings showed higher rates (2:40 1:42 mm3 per day vs 0:76 0:54 mm3 per day, mean standard deviation for A. caven and P. nigra, respectively; n ¼ 59; P < 0:01).
A. caven seedlings have shown higher number of leaves through the time considered (Fig. 8). The ANOVA test indicated that leaf production rate was significantly higher for A. caven seedlings (0:05 0:04 and 0:16 0:06 leaves per day for P. nigra and A. caven, respectively; P < 0:01). Final survival percentages also showed significant differences. Nearly all germinated A. caven seeds survived at least 50 days and the final survival percentage
Fig. 6. Mean values for stem height (mm) of P. nigra (~) and A. caven (&) seedlings (n ¼ 59). Table 3 Mean standard deviation values for stem height (mm) of P. nigra and A. caven seedlings (n ¼ 59) Stem height (mm) 10 days P. nigra A. caven P *
13.20 3.57 13.08 3.85 >0.7
20 days
30 days
40 days
50 days
60 days
16.43 3.34 19.67 4.76 <0.01*
26.92 8.06 31.46 8.97 <0.01*
36.41 10.76 46.07 11.58 <0.01*
46.71 14.07 60.28 15.54 <0.01*
59.51 18.11 80.27 22.11 <0.01*
Significant differences between species.
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Fig. 7. Volume of stems (mean values corresponds to seedlings that survived until the 60th day). Values for P. nigra (~) and A. caven (&) were fitted to lineal functions.
Fig. 8. Mean number of leaves. Values for P. nigra (~) and A. caven (&) were fitted to linear functions.
of A. caven seedlings was significantly higher than the corresponding figure for P. nigra (86.77 and 67.24%, respectively; Gauss test e ¼ 3:26; P < 0:01).
4. Discussion P. nigra seeds were adversely affected by waterimmersion, indicating perhaps that an increase in
waterlogging periods might affect new recruits of P. nigra thus altering the dominance pattern of this community woody layer. Because of the edaphic conditions of the area, surface horizon compaction due to cattle trampling might have a crucial influence on the soil water retention capacity because of the low permeability in the underlying horizon. An exceedingly high compaction might entail a change in soil response to equally intense
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precipitation, generating thus long waterlogging periods and, consequently, negative effects on P. nigra seed germination. The results obtained in this study suggest that a high animal load might have a differential effect on regeneration for the two species involved, since waterlogging due to cattle trampling might have dangerous effects for P. nigra germination and minimal effects on A. caven. Although P. nigra fruit ingestion by the greater rhea negatively affected final germination percentages, it also decreased the time required for germination. This may be due to digestion damage on the endocarp cover, a process that exposes the seed and favors water absorption once faeces are eliminated. Therefore, surviving seeds might germinate sooner and it might constitute an escape strategy against rodent and insect predation. Thus, the role of the greater rhea in this species regeneration might be substantial, since seed predation has been indicated as a decisive factor on the population dynamics of the Prosopis genus (Solbrig and Cantino, 1975; Villagra, 2000). Besides, fruit ingestion might keep up seed germination capability over longer periods of time. It has been remarked that P. nigra seeds are attacked by various internal parasites, especially insect larvae of the Bruchidae family, such as Rhipibruchus picturatus Fahr., R. prosopis King., and at least three different species of the Scutobruchus genus (Kingsolver et al., 1977). According to some authors (Janzen, 1969; Hauser, 1994; Miller, 1996), the digestive fluids of frugivorous animals might be lethal for parasite larvae, thus preventing the development of adult insects that lay eggs on healthy seeds. However, since this process has not been proven yet for P. nigra seeds ingested by the greater rhea, no detailed analysis of the mechanism involved in germinating power preservation through this frugivorous animal is provided. Studies on different species of the Prosopis genus indicate that their growth is extremely slow during the earlier stages of development (Catala´ n et al., 1994; Orfila, 1995; Felker, 1996) and that, under natural conditions, seedlings show very low survival percentages (Scifres and Brock, 1970a, 1970b). In this study, P. nigra seedling survival was low, even for experimental conditions, and even lower figures can be expected under natural conditions where hydric stress and the herbivorous habits of neighboring
23
animals are important mortality factors. Considering the high mortality rate, it might be assumed that a high number of recruits depends to a great extent on the successful germination of a similarly great number of seeds. Thus, unfavorable conditions for germination might implies that no seed produced in a certain year develops into a recruit. A. caven seedlings quickly develop a stronger structure that results in higher survival percentages. When compared to P. nigra seedlings, those of A. caven show some characteristics that may involve significant competitive advantages for establishment, such as a swift stem elongation and a high leaf production rate. Thus, A. caven seeds that succeed in germinating may have a higher probability of generating recruits.
5. Conclusion Various studies have shown the importance of different Prosopis species in ecosystems because they generate specific conditions that favor associated animal populations and plant communities (Kingsolver et al., 1977; Mares et al., 1977). These evidences suggest that P. nigra woods in the study area play a significant role in maintaining the structure and working order of the landscape by creating patches of specific physiognomy and composition, which constitute an habitat and food source for many wildlife species. This landscape may be preserved throughout time by taking into account the early development stage characteristics of P. nigra, the dominant species in slightly disturbed areas, and also of A. caven, the most favored species in highly disrupted areas. According to the results herein discussed, maintaining favorable conditions for P. nigra germination seems crucial for regenerating this species. Moreover, overgrazing appears as a decisive factor, not only because of its direct consequences on seedling and recruit consumption, but also because it highly modifies the soil permeability.
Acknowledgements We wish to thank Mr. I. Schojett for allowing the study to be conducted on his ranch, and S. Arias, J. Pereira, V. Cirelli, N. Fracassi, M. Biondini and M.
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Srur for their field support. A special thanks to the anonymous reviewers for constructive criticism. This research was carried forth through the TX-16 grant of the UBACyT Program of the Buenos Aires University and PICT 98 no. 04503 grant of the FONCYT Program of the Agencia de Promocio´ n Cientı´fica y Tecnolo´ gica.
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