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A comparative study of resource allocation in Pteridium in different Brazilian ecosystems and its relationship with European studies/Estudo comparativo da alocacao de recurso em Pteridium em diferentes ecossistemas brasileiros e sua relacao com estudos na europa.


Pteridium is a cosmopolitan genus that acts as an invasive species in many parts of the world. Most research on this genus has occurred in Europe, and there is a lack of data on it from South America, in spite of causing considerable conservation problems. We compared the biomass allocation of P. esculentum subsp. arachnoideum in two ecosystems in Brazil--Atlantic forest and Brazilian savanna. We measured the biomass of fronds, rhizomes and above-ground litter. We also compared the density, length and biomass of fronds from this Brazilian study with similar data of P. esculentum subsp. arachnoideum derived from Venezuela and P. aquilinum from Europe. P. esculentum subsp. arachnoideum showed a wide response range. We found a negative relationship between frond and necromass , indicating a negative feedback effect, while a positive relationship was observed between frond and rhizome biomass. The continental comparison of relationships showed that Pteridium responds in a different way in both Brazil and Europe, and that in Brazil fronds tend to be longer and heavier, presumably as a result of the continuous growing season in South America while is shortened in Europe by frost. The paper shows the ability of Pteridium to adapt to different ecosystems.

Keywords: bracken, resource partitioning, Atlantic Forest, Cerrado, biomass.


Pteridium e um genero cosmopolita que inclui especies invasoras em varias partes do mundo. Os estudos sobre o genero tem ocorrido principalmente na Europa, e existem poucas informacoes para as especies que ocorrem na America do Sul. Nesse estudo comparamos a alocacao de biomassa de P. esculentum subsp. arachnoideum em dois ecossistemas brasileiros--Mata Atlantica e Cerrado--em cada um dos quais medimos a biomassa nos rametas, nos rizomas e na serapilheira. Comparamos, tambem, a densidade, comprimento e biomassa dos rametas com informacoes obtidas sobre P. esculentum subsp. arachnoideum na Venezuela e P. aquilinum na Europa. P. esculentum subsp. arachnoideum apresentou respostas distintas. Encontramos uma relacao negativa entre a biomassa de rametas e da serapilheira, indicando uma retro-alimentacao negativa, enquanto houve uma relacao positiva entre a biomassa dos rametas e dos rizomas. A comparacao das relacoes entre os continentes indicou que Pteridium responde diferentemente no Brazil e na Europa, e tambem que no Brasil os rametas sao maiores e contem mais biomassa, possivelmente devido a estacao de crescimento continua, enquanto na Europa o crescimento e limitado pelas baixas temperaturas. Esse estudo demonstra o sucesso adaptativo de Pteridium em diferentes ecossistemas.

Palavras-chave, samambaiao, alocacao de recursos, Mata Atlantica, Cerrado, biomassa.

1. Introduction

Considering the impact that invasive species has been put on biological diversity all over the world, understanding how these species colonize successfully different ecosystems is a central goal in ecology. Invasive plant species, for example, are able to maintain or even increase its fitness across a range of environmental conditions through phenotypic plasticity (Richards et al, 2006; Rejmanek, 2011). Phenotypic plasticity refers to the ability of plants to modify its phenotype in response to environmental changes, with physiological and/or morphological adjustments at the individual level. Most classical examples of phenotypic plasticity are based on morphological traits: variations of leaves in response to variation of sun exposure (Bradshaw, 1963); changes on root growth in response to different concentrations of nutrients in heterogeneous soils (Miner et al., 2005; Jimenez-Ambriz et al., 2007); and differences in resource allocation, through changes in the allometric trajectories in response to environmental conditions (Carnier, 1991; Fan et al., 2009; Weiner, 2004).

Despite the controversial about resource allocation strategies (McConnaughay and Coleman, 1999; Fan et al., 2009), two main hypothesis have been proposed to describe biomass allocation (Muller et al., 2000; Shipley and Meziane, 2002; Niklas, 2005; McCarthy and Enquist, 2007; Yang et al., 2009); 1) the optimal partitioning hypothesis considers that plants allocate proportionally more biomass to a given organ to maximize their growth in response to environmental changes (Yang et al., 2009), while according to 2) the isometric allocation hypothesis the allocation does not change in response to environmental variations (Niklas, 2005; Yang et al., 2009). Thus, considering the relationship between the above and belowground biomass, the slope of the regression is 1.0 in case of isometric partitioning and variable for the optimal partitioning pattern.

Variations on biomass allocation can affect survival, growth and reproduction of individual plants and consequently shape the establishment and invasiveness in different habitats. Pteridium is a cosmopolitan genus occurring in a wide range of habitats worldwide, except in the polar regions (Marrs and Watt, 2006). Over much of its range it is a serious weed problem. Although a great deal is known about Pteridium ecology, its form and function, and control measures, most of this has been derived from studies in Europe about Pteridium aquilinum (?.) Kuhn (Marrs and Watt, 2006), and until recently there has been much less data from South America (Alonso-Amelot and Rodulfo-Baechler, 1996; Thomson and Alonso-Amelot, 2002; Hartig and Beck, 2003; Alonso-Amelot and Oliveros-Bastidas, 2005; Silva and Silva Matos, 2006; Silva Matos and Belinato, 2010; Miatto et al., 2011). This lack of data from South America is surprising because Pteridium esculentum arachnoideum abundance is causing concern for animal health across the continent (Franca et al., 2002; Marcal et al., 2002; Marcal, 2003). Thus, from both ecological and economic viewpoints there is a need to collect data on P. esculentum subsp. arachnoideum from South America and to relate this to the existing data available from Europe. This comparison would clearly facilitate the exchange of management practices for controlling this aggressive weed. The ideal way to study species performance across regions in the first instance is to compare biomass allocation data. Accordingly, here the allocation strategies of Pteridium were measured in Brazil, and compared to available literature data derived from elsewhere in South America, but mainly from the Europe. We looked for patterns of correlations in biomass allocation between two major plant pools that could reflect functional linkages between some species attributes. Such allocation differences would result because resource allocation to one organ or function would not be available for use by other organs or functions (Stuefer et al., 2002; Weiner, 2004).

In temperate climates Pteridium produces large stands with a dense canopy of green fronds, recruitment is rare in nature; patch expansion is achieved by vegetative growth through the rhizomes, the rate of frond decomposition is low and the litter layer can be very deep (Marrs and Watt, 2006). Whilst litter would normally be considered as part of the necromass, it provides a major ecological function for the species in terms of modification of the microclimate through frost protection (Marrs and Watt, 2006) and in suppressing the ingress of other species (Ghorbani et al., 2006; Marrs and Watt, 2006). We hypothesized that as Pteridium is considered an aggressive and invasive plant, changes in biomass allocation would be expected due to climatic differences representing the adaptation of this genus to occupy different ecosystems. In this case the optimal partitioning hypothesis (Yang et al., 2009) would be accepted. Therefore, we aimed to answer the two following questions; (1) is the biomass allocation similar in two contrasting Brazilian ecosystems? (2) Are the European and South American Pteridium comparable, so that management control strategies derived in one region might be applicable elsewhere?

2. Material and Methods

2.1 Measurement of biomass allocation in Pteridium esculentum subsp. arachnoideum

Pteridium esculentum (G. Forst.) Cockayne subsp. arachnoideum (Kaulf.) J. A. Thomson, Dennstaedtiaceae, is a neotropical species within the Pteridium genus found in Brazil, according to Thomson (2012). The biomass of this species was sampled from july to September in two different Brazilian ecosystems, Atlantic Forest and Cerrado (hereafter named as Savanna) located in eight biological reserves (see Table 1). The Atlantic Forest is one of world most luxurious and important ecosystems for conservation because of its high biodiversity and high proportion of endemic species (Myers et ah 2000). Nowadays, it is reduced to 8% of its original area (Fundacao SOS Mata Atlantica; INPE, 2009). Brazilian Savanna is the world's most biologically-rich savanna ecosystems (The Nature Conservancy, 2010); originally it occupied 21% of the Brazilian territory (about 2 million [km.sup.2]), however at least 48% percent of it has already been severely degraded (Pereira and Gama, 2010). In both ecosystems, P. esculentum subsp. arachnoideum has been described as invasive affecting the structure of their plant community Silva Matos et ah 2002,2005; Silva and Silva Matos 2006; Silva Matos and Belinato, 2010; Miatto et al., 2011).

Within eight biological reserves covering the two ecosystems (Atlantic rain forest, n=4; Savanna, n=6, see Table 1), ten sites covered by P. esculentum subsp. arachnoideum were identified. Within each site, five replicate sampling positions were located randomly. At each of these positions a 0.5 x 0.5 x 0.5 m quadrat was positioned and all living fronds and litter biomass (hereafter named as necromass) was harvested, and the length of all fronds were measured. In this paper, we will hereafter use the term frond to represent collectively all fronds from each individual position. A soil pit was then dug and all rhizomes were removed by hand from the excavated soil and washed free of surface soil; the quality assurance procedure for rhizome sampling of Le Due et al. (2003) was followed. Both frond and rhizome samples were then dried at 80[degrees]C for 48 h and weighed.

2.2 Assessment of literature data on biomass allocation in Pteridium

In order to compare the Brazilian data with data obtained from other regions of the world, a Systematic Review using two literature databases was perfonned (Web of Science, Google Scholar), using "bracken" and "Pteridium" as key search terms. All papers identified were inspected, and a subset of papers that included data on biomass allocation was selected and the biomass data abstracted (see Table 2). Most papers contained data on the above-ground components; there was much less information about rhizomes so that comparisons were not viable.

2.3 Data analysis

Differences in P. esculentum subsp. arachnoideum performance between Brazilian ecosystems (Atlantic Forest and Savanna) were assessed between ecosystems using two-sample t-test with pooled variances of the Systat statistic package. In order to cope with errors on both axes and doesn't assume which is the dependent variable, reduced major axis regressions (RMA) were estimated to data derived from the two ecosystems using PAST (Hammer el al., 2001) and Spearman's correlation coefficients were calculated to assess the significance of these relationships. The comparisons of the slopes were performed through the analysis of covariance for RMA. using the significance of the Bartlett-corrected likelihood ratio statistic testing for common slope (LR), within the R statistical environment (R v.2.10.1, R Development Core Team, 2004).

In order to assess differences in resource partitioning, RMA regressions were fitted to the South American and European data (data abstracted from references in Table 2). The linear regressions obtained were compared through analysis of covariance as described above. The relationships were derived from the mean values for each variable at each site; where only a range was reported the average of the minimum and maximum value was used.

3. Results

3.1 Biomass allocation in Brazilian P. esculentum subsp. arachnoidenm

There were no significant differences between the ecosystems for all variables: frond biomass, rhizome biomass, necromass, frond density, and frond length (see Table 3). Frond biomass was very variable in the Savanna and in the Atlantic Rain Forest, ranging from 114-2353 g [m.sup.-2] and from 284-1912g [m.sup.-2], respectively. A similar pattern was found for necromass (Savanna = 0-2970 g [m.sup.-2]; Atlantic Rain Forest = 213-2264 g [m.sup.-2]). Leaf density and rhizome biomass, however, did not show as extreme a pattern as these other two variables. Savanna still had the greatest variability (1-28 leaves [m.sup.-2]) overlapping the ranges of the Atlantic Rain Forest (4-20 leaves [m.sup.-2]), and rhizome biomass ranging from 23.5 to 2757 g [m.sup.-2] in the Savanna and from 219 to 1477 g [m.sup.-2] in the Atlantic Rain Forest. Length of expanded leaf ranged from 0.5 to 4.2 m in the Savanna, and from 1 to 4.1 m In the Atlantic Rain Forest.

When all data were combined, significant positive relationships were found between: (1) frond and rhizome biomass and (2) frond biomass and necromass, while no relationship was observed between the rhizome/frond biomass ratio and necromass (see Table 4). Additionally, considering the ecosystem types, positive relationships were significant only for the Savanna (see Figure 1, Table 4).

There were no significant ecosystems differences in the slopes of the relationship between (1) rhizome and frond biomass (LR=3.050, p=0.080), (2) rhizome biomass and necromass (LR= 1.056, p=0.304), and (3) leaf density and frond biomass (LR=0.749, p=0.387). On the other hand, there were significant differences in the slopes of the relationships between (1) frond biomass and necromass (LR=6.651, p=0.010), albeit weakly, (2) rhizome/frond biomass and necromass (LR=7.900, p=0.005) and (3) frond biomass and total biomass (LR=4.186, p=0.041).

3.2 Comparison of biomass allocation in Pteridium between South-America and Europe

A comparison of absolute values (see Table 2) showed that frond density is, in general, greater in Europe than in South America (t-test, t= 2.55, p= 0.015). Flowever, leaf length (t= 2.82, p= 0.007), frond biomass (t= 4.0, p= 0.002), and leaf biomass (t= 8.04, p< 0.001), calculated by dividing the total frond biomass (g [m.sup.-2]) by leaf density (leaves [m.sup.-2]), were significantly greater in the South American samples. The range of frond lengths from both regions showed substantial overlap, but the European fronds were in the lower part of the range and the South American fronds in the upper part.

The relationship between European variables indicated a negative significant relationship between (1) leaf density and leaf length and (2) leaf length and leaf biomass, whereas a positive relationship was detected between leaf density and leaf biomass (see Figure 2 and Table 4). We observed significant relationship for data from South America only between density and leaf biomass (LR=11.903, p=0.0006). There was no significant difference in the slope for the relationship between (1) leaf length and leaf biomass (LR=2.318, p= 0.128) and (2), leaf density and leaf length (LR=0.256, p=0.613) (see Figure 2).

4. Discussion

4.1. Biomass allocation

In Brazil Pteridium esculentum subsp. arachnoideumis is found in both Atlantic Forest and Savanna, suggesting that this species is able to colonize contrasting ecosystems habitat. There were no significant differences in frond biomass, frond length, frond density and litter biomass, but the significant differences found on the variances, in general greater in the Savanna, indicated differences between study sites rather than ecosystems. Because of its large area, Savanna includes a high diversity of soil types, climate and vegetation types (Silva et al., 2006). We could expect such variation as a function of these environmental heterogeneity.

It has been suggested that the development of a complex rhizome system requires a substantial investment and with this comes a considerable measurable risk (de Kroon and van Groenendael, 1997). Our results suggest that a common rhizome mass is able to support a large variation in frond biomass, which can be expressed through differences in both frond density and frond length. In tropical areas we could expect more investment in above-ground biomass, as frond longevity is greater as a consequence of the less harsh climate and hence productivity should also be greater.

Environmental heterogeneity in tropical ecosystems, in terms of canopy coverage, may be a factor determining the above-ground biomass variation, considering that individual ramets have to struggle for light, to maintain the productivity of the overall clone (Huber and Hutchings, 1997).

In terms of vegetation dynamics two important results were obtained. The first was the negative relationship between frond and litter biomass found to Atlantic Forest data, indicating that the dense litter layer developing under the P. esculentum subsp. arachnoideum may be harmful for its own regeneration, as first suggested by Watt (1945, 1947, 1976) as well as for other species (Marrs, 1988; Marrs et al., 2007). The second was the dense canopy of P. esculentum subsp. arachnoideum fronds which is also an important factor contributing to its ability to become a dominant species and being able to prevent the colonization by other species (Marrs, 1988; Marrs and Pakeman, 1995; Ghorbani et al., 2006). Both dense canopy cover and depth litter layer can also get one further problem with Pteridium colonization: the impoverishment of the soil seed bank (Ghorbani et al, 2006). A reduction in species present in the seed bank of Atlantic Forest was found in a previous study (Silva and Silva Matos, 2006).

Another direct consequence of such a deep litter layer (necromass) is that the risk and intensity of fire is increased in both ecosystems. Normally, natural fires occur in the Savanna every two to three years (Hoffmann, 1996), but nonnatural, human-induced fires are increasingly common albeit unpredictable including in the moist Atlantic Forest (Silva Matos et al., 2002,2005). Unfortunately, the relationship of P. esculentum subsp. arachnoideum and fire in the Savanna is still unclear, but we might hypothesize that a positive feedback of fire on P. esculentum subsp. arachnoideum will develop: fire keeps the woody vegetation under control which allows P. esculentum subsp. arachnoideum to spread increasing its biomass, which in turn increases the risk, intensity and frequency of fire events, leading to the decrease in the biological diversity changing the structure of the community (Hoffmann and Moreira, 2002; Pivello, 2006).

These results are worry ing because these are both ecosystem types of considerable international conservation importance (Myers et al., 2000) and the P. esculentum subsp. arachnoideum here exhibits a very large range of allocation responses, implying considerable plasticity, and hence must be viewed as a major potential future invasive threat.

4.2. Comparison of biomass allocation between European and South American Pteridium

Different biomass allocation strategies were detected between European and South American Pteridium. In Europe, the frond life-cycle is expected to last at most seven months in any given annual season because all fronds are killed by winter frost (Pakeman, et al., 1994; Pakeman and Marrs, 1996; Pother, et al., 2005; Marrs and Watt, 2006), and there should therefore be less investment in fronds, in terms of biomass/length and biomass/density. In tropical South America, by the other hand, we could expect an increase of leaf biomass after the maximum length is attained as leaves live longer than in Europe. However, the higher slope observed in the leaf density x leaf biomass relationship for the South America data, indicates that the increase of fronds causes a negative effect on the biomass allocation of P. arachnoideum. According to Weiner (2004) environmental selection pressures drive changes on plant resource allocation. So, in a large-scale comparison, between Brazil and Europe, we can assume that differences on the biomass allocation patterns resulted from different climate pressures and speciation, while in the comparison of Brazilian ecosystems such pattern resulted from small-scale environmental heterogeneity, as discussed earlier. This broad plasticity might have allowed Pteridium to develop as an invasive genus in diverse bioclimatic regions.

For the conservation of endangered ecosystems Pteridium poses substantive actual and potential threats (Pakeman and Marrs, 1992). Its wide geographic range coupled with the environmental plasticity demonstrated here allows it to succeed in a wide range of habitats, and also makes it difficult to predict its invasiveness (Goodwin et al., 1999). As the Pteridium patch increases mainly through rhizome expansion (Marrs and Watt, 2006), it should be possible to control it by manipulating resource allocation between the rhizomes and fronds. In Europe, frond removal by cutting and other mechanical treatments is used routinely to control Pteridium. A similar approach should be even more effective in South America where there is a greater proportion of the resource allocated to the production of a large frond biomass. However, this strategy needs to be tested experimentally.


Acknowledgements--We thank S. Matos, A. Matos, M. Matos, A. Muller, P. Dodonov, A. de Paula, T. Sampaio e Silva, I. Silva, R. Miatto, C. Zanelli and L. Joaquim for help with field work, CNPq and FAPESP for scholarships (CNPq. R.O. Xavier) and (FAPESP, D.M. Silva Matos 2007/05658-3; F.C.S. Tiberio, 2007/07976-2, and FAPESP for part funding this project (2006/61570-5).


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Silva Matos, DM. (a) *, Xavier, RO. (a), Tiberio, FCS. (a) and Marrs, RH. (b)

(a) Departamento de Hidrobiologia, Universidade Federal de Sao Carlos--UFSCar, Rod. Washington Luis, Km 235, CP 676, CEP 13565-905, Sao Carlos, SP, Brazil

(b) School of Environmental Sciences, University of Liverpool, Liverpool, L69 3GP, UK

* e-mail:

Received: October 5, 2012--Accepted: December 3, 2012--Distributed: February 28, 2012 (With 2 figures)

Table 1. Description of the ten study sites across the two Brazilian

                                         Longitude,         Altitude
Ecosystem   Study site location           latitude            (m)

Atlantic      Parque Estadual       S 24[degrees]04' 23"      710
Forest         Carlos Botelho       W 47[degrees]59' 52"

              Parque Estadual      S 24[degrees]39' 029"       12
                 Campina do        W 47[degrees]49' 835"
              Encantado (PECE)

              Parque Estadual      S 24[degrees]30' 146"      548
               de Jacupiranga      W 47[degrees]50' 303"

              Parque Estadual       S 25[degrees]12' 45"       5
              Ilha do Cardoso       W 47[degrees]59' 48"

Savanna      Reserva de Cerrado    S 21[degrees]57' 971"      860
            da UFSCar, adjacent    W 47[degrees]52' 150"
              to the riparian
              forest (UFSCarl)

             Reserva de Cerrado    S 21[degrees]58' 125"      866
            da UFSCar 800m from     W 47[degrees]51 882"
            the riparian forest
                 (UFSCar 2)

             Estacao Ecologica     S 22[degrees]12' 382"      737
             de Itirapina (EEI)    W 47[degrees]55' 840"

             Parque Estadual de      S 21[degrees]50'         540
               Porto Ferreira        W 47[degrees]28'

            Reserva Biologica do   S 15[degrees]56' 394"      1120
              IBGE (Brasilia)      W 47[degrees]51' 960"
                 (RECOR 1)

            Reserva Biologica do   S 15[degrees]56' 313"      1135
              IBGE (Brasilia)      Wo 47[degrees]52' 026"
                 (RECOR 2)

                                   Climate Mean
Ecosystem   Study site location      (mm/year)     Soil description

Atlantic      Parque Estadual          18-20        Hydromorphic,
Forest         Carlos Botelho       1,500-2,200       yellow-red
                   (PECB)                            latosols and

              Parque Estadual         17.5-27        Quartzarenic
                 Campina do         1,600-2,200         Neosol
              Encantado (PECE)

              Parque Estadual          17-35        Flydromorphic,
               de Jacupiranga       1,600-2,200       yellow-red
                   (PEJ)                             latosols and

              Parque Estadual          21.2          Sandy soils
              Ilha do Cardoso          3,000

Savanna      Reserva de Cerrado        22.1        Alie red-yellow
            da UFSCar, adjacent        1,339        and distrophic
              to the riparian                         red-yellow
              forest (UFSCarl)                         latosols

             Reserva de Cerrado        22.1        Alie red-yellow
            da UFSCar 800m from        1,339        and distrophic
            the riparian forest                       red-yellow
                 (UFSCar 2)                            latosols

             Estacao Ecologica         22.0          Quartzarenic
             de Itirapina (EEI)        1,339            Neosol

             Parque Estadual de      17.2-22.8        Distrophic
               Porto Ferreira          1,300          red-yellow
                   (PEPF)                              latosols

            Reserva Biologica do        23             Dark-red
              IBGE (Brasilia)          1,527           latosols
                 (RECOR 1)

            Reserva Biologica do        23             Dark-red
              IBGE (Brasilia)          1,527           latosols
                 (RECOR 2)

Table 2. Comparative dataset on Pteridium biomass allocation derived
from the literature from Europe, South America and this study.

                                      Leaf density   leaf length
Region           Site/ecosystem       ([m.sup.2])       (cm)

Europe       Bealieu heath                 --            --
             Stony Cross                   --            --
             North Bentley                 --            --
             South Bentley                 --            --
             Bowland Forest                --            --
             Lakenheath grassland A       1.5           31.5
             Lakenheath grassland B       2.95          35.5
             Lakenheath grassland C      22.85           64
             Lakenheath grassland D      50.25           125
             Lakenheath grassland E      31.05          47.5
             Weeting                       23           142.5
             Cavenham                      24            100
             Stanford PTA. Norfolk         35
             Mull                          32           132.1
             Sourhope                     31.5           87
             Lake District                32.5          71.5
             Clywd                        28.5           111
             Breckland                     31           76.5
             Devon                        15.5           113
             Lindale                       --            --
             Sourhope 1                   58.8          56.5
             Souhope 2                    26.5          69.9
             Peak                         42.6          91.1
             Carneddau                     44           74.1
             Cannock 1                    36.8          105.9
             Cannock 2                    29.7          73.7
             Open                         15.4           245
             Larix woodland               8.1            241
             Larix woodland               8.5            216
             Larix woodland               6.1            203
             Larix woodland               6.2            193
             Larix woodland               6.4            165
             Pinus woodland                7             210
             Pinus woodland               3.1            213
             Pinus woodland               12.9           129
             Ouercus woodland             3.4            174
             Querais woodland             3.7            216
             Quercus woodland             3.9            176
             Ouercus woodland             4.4            136
S. America   Venezuelan montane           5.1            89
             Venezuelan montane           1.6           76.59
             EE1                          20.4           146
             PEPF                         17.6           231
             RECOR1                       9.6            243
             RECOR2                       4.6            147
             UFSCar1                      13.6           321
             UFSCar2                      10.4           180
             PEJ                          19.2           190
             PECE                         10.4           288
             PEIC                         20.0           184
             PECB                         10.4           209

                                      Frond biomass
Region           Site/ecosystem       (g [m.sup.-2])

Europe       Bealieu heath                 892
             Stony Cross                   1408
             North Bentley                 1072
             South Bentley                 848
             Bowland Forest                1104
             Lakenheath grassland A        5.9
             Lakenheath grassland B        15.5
             Lakenheath grassland C       183.5
             Lakenheath grassland D       923.5
             Lakenheath grassland E       167.5
             Weeting                       520
             Cavenham                      385
             Stanford PTA. Norfolk         590
             Mull                          533
             Sourhope                     382.5
             Lake District                 346
             Clywd                         546
             Breckland                     371
             Devon                         322
             Lindale                       985
             Sourhope 1                   391.3
             Souhope 2                    297.5
             Peak                         521.9
             Carneddau                    537.6
             Cannock 1                    676.4
             Cannock 2                    294.2
             Open                         731.1
             Larix woodland               313.5
             Larix woodland               316.5
             Larix woodland               207.7
             Larix woodland               136.8
             Larix woodland               175.9
             Pinus woodland               234.2
             Pinus woodland               101.9
             Pinus woodland               177.8
             Ouercus woodland              79.4
             Querais woodland             135.4
             Quercus woodland             104.4
             Ouercus woodland              79.7
S. America   Venezuelan montane           287.4
             Venezuelan montane            53.2
             EE1                         1,236.0
             PEPF                        1,448.8
             RECOR1                       481.2
             RECOR2                       522.0
             UFSCar1                     1,178.9
             UFSCar2                      933.9
             PEJ                         1,610.0
             PECE                         817.3
             PEIC                        1,179.4
             PECB                         951.9

Region           Site/ecosystem                 Source

Europe       Bealieu heath            Pearsall and Gorham (1956)
             Stony Cross              Pearsall and Gorham (1956)
             North Bentley            Pearsall and Gorham (1956)
             South Bentley            Pearsall and Gorham (1956)
             Bowland Forest           Pearsall and Gorham (1956)
             Lakenheath grassland A   Watt (1964)
             Lakenheath grassland B   Watt (1964)
             Lakenheath grassland C   Watt (1964)
             Lakenheath grassland D   Watt (1964)
             Lakenheath grassland E   Watt (1964)
             Weeting                  Lowday and Marrs (1992)
             Cavenham                 Marrs et al. (1998)
             Stanford PTA. Norfolk    Pakeman and Marrs (1994)
             Mull                     Paterson et al. (1997)
             Sourhope                 Paterson et al. (1997)
             Lake District            Paterson et al. (1997)
             Clywd                    Paterson et al. (1997)
             Breckland                Paterson et al. (1997)
             Devon                    Paterson et al. (1997)
             Lindale                  Lawson et al. (1986)
             Sourhope 1               Le Due et al. (2000)
             Souhope 2                Le Due et al. (2000)
             Peak                     Le Due et al. (2000)
             Carneddau                Le Due et al. (2000)
             Cannock 1                Le Due et al. (2000)
             Cannock 2                Le Due et al. (2000)
             Open                     den Ouden (2000)
             Larix woodland           den Ouden (2000)
             Larix woodland           den Ouden (2000)
             Larix woodland           den Ouden (2000)
             Larix woodland           den Ouden (2000)
             Larix woodland           den Ouden (2000)
             Pinus woodland           den Ouden (2000)
             Pinus woodland           den Ouden (2000)
             Pinus woodland           den Ouden (2000)
             Ouercus woodland         den Ouden (2000)
             Querais woodland         den Ouden (2000)
             Quercus woodland         den Ouden (2000)
             Ouercus woodland         den Ouden (2000)
S. America   Venezuelan montane       Alonso-Amelot and
               savanna                  Rodulfo-Baechler (1996)
             Venezuelan montane       Alonso-Amelot and
               savanna                  Rodulfo-Baechler (1996)
             EE1                      This study
             PEPF                     This study
             RECOR1                   This study
             RECOR2                   This study
             UFSCar1                  This study
             UFSCar2                  This study
             PEJ                      This study
             PECE                     This study
             PEIC                     This study
             PECB                     This study

Tabic 3. Biomass allocation in P. esculentum subsp. arachnoideum
stands of different Brazilian ecosystems. Mean [+ or -] SE, t-values
and significance (p) values are presented;

Variable                         Savanna

Frond biomass              966.8 [+ or -] 104.9
Rhizome biomass *          696.3 [+ or -] 121.7
Total biomass             1663.1 [+ or -] 183.8
Leaf biomass *              88.5 [+ or -] 11.7
Density of leaves           12.7 [+ or -] 1.2
Rhizome/frond biomass *      0.8 [+ or -] 0.15
Leaf length *                2.1 [+ or -] 0.11
Necromass *               1073.1 [+ or -] 161.6

Variable                     Atlantic Forest       t       P

Frond biomass             1139.6 [+ or -] 116.8   1.08   0.286
Rhizome biomass *          795.2 [+ or -] 85.4    0.60   0.964
Total biomass             1934.8 [+ or -] 171.1   1.02   0.311
Leaf biomass *              93.4 [+ or -] 7.5     0.33   0.742
Density of leaves           12.8 [+ or -] 1.3     0.04   0.964
Rhizome/frond biomass *      0.9 [+ or -] 0.15    0.31   0.760
Leaf length *                2.1 [+ or -] 0.08    0.21   0.831
Necromass *                964.2 [+ or -] 128.1   0.53   0.600

* indicates unequal variances according to Levene's test (p<0.05).
Biomass and necromass are given in g/[m.sup.2], density as the number
of individual fronds/[m.sup.2] and mean frond length in m. Fronds
were considered as the whole group of leaves sampled at each plot.
Number of samples was 30 for Savanna and 20 for the Atlantic Forest;
75 leaves were measured in the Atlantic Forest and 82 in Savanna.

Table 4. Parameters of the reduced major axis regression estimated
for data illustrated in (a) Figure 1 and (b) Figure 2. Spearman's
correlation coeficients ([r.sub.s]) and significance (p) are presented.

(a) Number of samples was 30 for Savanna and 20 for the Atlantic
Forest, all analyses were performed using In transformed data.

Variables          Ecosystem           a       b     [R.sup.2.

Frond biomass vs   Combined          0.65    1.18          0.32
Rhizome biomass    Savanna           0.60    3.05          0.38
                   Atlantic Forest   1.00    0.38          0.09

Rhizome            Combined          0.77    0.95          0.17
  biomass/Frond    Savanna           0.93    -6.89         0.334
  biomass vs       Atlantic Forest   1.01    -7.15         0.137

Frond biomass      Combined          0.97    -3.05         0.27
vs Necromass       Savanna           0.72    1.80          0.33
                   Atlantic Forest   -0.85   12.61         0.04

Variables          Ecosystem         [r.sub.s]      P

Frond biomass vs   Combined            0.437      0.002
Rhizome biomass    Savanna             0.614     <0.001
                   Atlantic Forest     0.308      0.186

Rhizome            Combined            0.227      0.121
  biomass/Frond    Savanna             0.578      0.021
  biomass vs       Atlantic Forest     0.370      0.108

Frond biomass      Combined            0.548     <0.001
vs Necromass       Savanna             0.618     <0.001
                   Atlantic Forest     -0.20      0.389

(b) Number of samples was 32 for Europe and 12 for the South America,
all analyses were performed using In transformed data.

Variables          Continent           a       b     [R.sup.2.

Leaf density vs    Europe            -0.54    6.16         0.08
  Leaf length      S. America         0.57    3.88         0.459

Leaf density vs    Europe             1.04    2.70         0.661
  Leaf biomass     S. America         1.26    3.65         0.898

Leaf length vs     Europe             1.89   -3.51         0.10
  Leaf biomass     S. America         2.21   -4.93         0.54

Variables          Continent         [r.sub.s]      P

Leaf density vs    Europe             -0.2758    0.12653
  Leaf length      S. America          0.677     0.0155

Leaf density vs    Europe              0.813     0.0001
  Leaf biomass     S. America          0.974     0.0001

Leaf length vs     Europe              0.321      0.073
  Leaf biomass     S. America          0.735      0.006
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Author:Silva Matos, D.M.; Xavier, R.O.; Tiberio, F.C.S.; Marrs, R.H.
Publication:Brazilian Journal of Biology
Date:Feb 1, 2014
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