Temporal dynamics of the superdominant bracken fern Pteridium arachnoideum in Neotropical savanna-riparian forest transitions

Abstract

Clonal growth can be especially advantageous in spatially heterogeneous environments and some clonal plants are highly invasive or superdominant, especially in disturbed environments. However, their temporal dynamics in the absence of large disturbances are not well known. We assessed whether patches dominated by the native bracken fern Pteridium arachnoideum expanded or retracted in area over six years. We mapped the contour of eight patches occupied by P. arachnoideum in a savanna-forest transition every two years from 2009 to 2015. The area occupied by most patches was overall stable, indicating that forested patch boundaries may be unsuitable for an effective vegetative spread of P. arachnoideum. One patch fully retracted during the study period, possibly due to extensive herbivory by leafcutter ants. Thus, although clonal foraging may enable the spread of the species to more suitable sites from these patches, these results indicate that P. arachnoideum does not represent a threat to the biodiversity of savanna-riparian forest transitions in the absence of extensive disturbances, as the area of the largest patches remained stable or decreased during our study. These findings highlight that specific characteristics of the local disturbance regime may be key to the cost-effective management of some superdominant native species.

Key words:
cerrado; clonal growth; disturbance; Pteridium esculentum subsp; arachnoideum; riparian forest

Resumo

O crescimento clonal tende a ser especialmente vantajoso em ambientes espacialmente heterogêneos e algumas plantas clonais são altamente invasivas ou superdominantes, especialmente em ambientes perturbados. No entanto, a sua dinâmica temporal na ausência de distúrbios maiores não é bem conhecida. Nós acompanhamos manchas dominadas pela samambaia nativa Pteridium arachnoideum ao longo de um período de seis anos para avaliar se elas aumentaram ou diminuíram de tamanho durante este tempo. Nós amostramos seis manchas ocupadas por P. arachnoideum em uma transição entre floresta e savana e mapeamos o seu contorno de dois em dois anos, de 2009 a 2015. Não houve incêndios na área de estudo durante este período e a área ocupada pela maioria das manchas se manteve no geral estável, indicando que limites de manchas de floresta parecem não serem adequadas para uma expansão vegetativa efetiva do P. arachnoideum. Além disso, uma mancha retraiu completamente durante o tempo de estudo, possivelmente devido a herbivoria intensa por formigas-cortadeiras. Assim, embora forrageamento clonal possa permitir o espalhamento desta espécie para sítios mais adequados a partir das manchas já ocupadas, estes resultados indicam que P. arachnoideum não é uma ameaça à biodiversidade em transições entre savana e floresta ripária na ausência de grandes distúrbios, já que a área das manchas permaneceu estável ou diminuiu durante o estudo. Estas descobertas enfatizam que decisões relacionadas ao manejo de espécies nativas superdominantes (e.g., controle ativo ou regeneração natural) devem considerar como estas espécies respondem ao regime local de distúrbios.

Palavras-chave:
cerrado; crescimento clonal; distúrbio; Pteridium esculentum subsp; arachnoideum; floresta ripária

Introduction

Figure 1
a. Satellite image showing the size and shape of patches dominated by the southern bracken (Pteridium arachnoideum) in a savanna-riparian forest transition in the Brazilian southeast (the shaded areas represent each patch with their maximum size during a 6-year monitoring period; the letters within or next to the patches correspond to the codes (unique identifiers) given to each patch). b-c. view from within the patches.

The ecological advantages of clonal growth have been extensively studied during the last decades, particularly for herbs from temperate plant communities (Pennings & Callaway 2000; Roiloa et al. 2010; Xu et al. 2010). Newly emerged modules (hereafter called ramets) of clonal species often receive stored resources previously produced by mature ramets, thus exhibiting high growth and survival rates and making these species more likely to occur where growing conditions are poor (Stuefer et al. 1994; Hutchings & Wijesinghe 1997; Amsberry et al. 2000). Clonal growth also enables certain stoloniferous and rhizomatous species to originate new patches by changing internode distance (spacing between ramets) and branching intensity according to local environmental conditions (De Kroon & Hutchings 1995; Duchoslavová & Weiser 2017). However, this local spread may be less effective where environmental conditions are more stable and spatially homogeneous (Hutchings & Wijesinghe 1997; Hutchings & Wijesinghe 2008). In addition, it may also depend on the efficiency and duration of the clonal integration (D’hertefeldt & Ingibjo 2003; Klimeš 2008), as well on the response to local environmental variation at the ramet level (Evans 1992; Dong 1993; Xu et al. 2010).

Clonal growth may favor the formation of large monospecific stands of native species, especially clonal perennial herbs (e.g., Amsberry et al. 2000; Griscom & Ashton 2006; Rother et al. 2009; Lima et al. 2012; Stevens et al. 2015). Even though these stands often occur in sites naturally subjected to either large disturbances or strong environmental filters (Walker 1994; Amsberry et al. 2000; Gagnon et al. 2007), they have also been found in diverse disturbed tropical rainforests as a result of large-scale natural disturbances or of anthropogenic activities (Griscom & Ashton 2003; Larpkern et al. 2011; Lima et al. 2012). Many of these clonal plants dominating tropical ecosystems are perennial species with efficient clonal growth, such as a number of bamboo species (Campanello et al. 2007; Larpkern et al. 2011; Lima et al. 2012) and ferns from the Pteridium genus (Marrs & Watt 2006). These mono-specific stands may persist for long periods, as, for some of these species, a single genetically identical individual (genet) has been shown to survive for hundreds to thousands of years (Marrs & Watt 2006), and conditions within the stand are often unsuitable for the establishment of other native species (Walker 1994; Rother et al. 2009; Larpkern et al. 2011).

Pteridium arachnoideum (Kaulf.) Maxon is considered a threat to the local biodiversity of certain disturbed Neotropical ecosystems, where its long-term persistence and expansion has been especially associated with fire occurrence (Hartig & Beck 2003; Silva & Silva Matos 2006; Portela et al. 2009; Roos et al. 2010; Menezes et al. 2019; Xavier et al. 2023). A better knowledge of its patch dynamics in the absence of disturbances, for example whether patches dominated by it tend to expand or to decrease in size, may aid decision making regarding the control of this species. We monitored for six years the variation in the size of patches dominated by P. arachnoideum in a Neotropical savanna-riparian forest transition protected from disturbances in South-eastern Brazil, in order to determine whether (1) Pteridum arachnoideum patches would enlarge, thus overthrowing the surrounding vegetation; (2) the patches would remain stable during the study period, indicating that this species is in equilibrium with the surrounding communities; or (3) the patches would diminish, being replaced by the surrounding vegetation. Degeneration of Pteridum patches has been identified at a time scale of decades (Marrs & Hicks 1986; Marrs & Watt 2006), and the growth of P. arachnoideum has been shown to be negatively affected by shading (Xavier et al. 2019). Accordingly, we expected that the patches would remain stable during the study period, corroborating with the definition of P. arachoideum as a native species that only becomes dominant under specific conditions.

Material and Methods

Study species

Several clonal ferns from the genus Pteridium are native in multiple ecosystems from all continents except Antarctica (Marrs & Watt 2006). Even though there are ecological differences among these species (Silva Matos et al. 2014), they produce an extensive rhizome system, so that visible aboveground parts are in effects emergent fronds (petiole and laminae) often connected underground (Marrs & Watt 2006). Such rhizome system allows for large resource storage and efficient translocation between fronds (hereafter referred to as ramets), thus being a major dispersion mechanism of these species, since sexual reproduction is rare (Marrs & Watt 2006). Once established, stands dominated by Pteridum exhibit a dense canopy and a deep litter layer (den Ouden 2000; Ghorbani et al. 2006), hampering the establishment of other species. Species from the genus are dominant in large degraded temperate (Marrs & Watt 2006; Stevens et al. 2015; Alday et al. 2023) and tropical ecosystems (Alonso-Amelot & Rodulfo-Baechler 1996; Hartig & Beck 2003; Silva Matos & Belinato 2010; Silva Matos et al. 2014; Menezes et al. 2019; Levi-Tacher & Morón-Ríos 2023; Xavier et al. 2023).

There are several synonyms for the common bracken ferns of south-eastern Brazil, such as Pteridium arachnoideum, P. aquilinum var. arachnoideum, P. esculentum subsp. arachnoideum, and P. esculentum subsp. arachnoideum var. arachnoideum (Schwartsburd et al. 2018). The most recent phylogenetic studies suggest a close relationship between the South American P. arachnoideum and the Australasian P. esculentum, thus supporting the name P. esculentum subsp. arachnoideum (Thomson 2012; Schwartsburd et al. 2018). Here, for practical reasons, we adopted the classification of P. arachnoideum at species level. P. arachnoideum is a rhizomatosous and perennial species, with fronds (ramets) reaching up to 3-4 m in height and with a leaf morphology clearly different from the northern bracken fern P. aquilinum (Thomson 2012; Xavier et al. 2019).

Study site

We performed this study in a transition area between a dense savanna and a riparian forest in São Carlos, São Paulo state, South-Eastern Brazil. Average annual precipitation and temperature are 1,500 mm and 21 °C, respectively. The area is located within the Federal University of São Carlos, between a riparian forest around a narrow second-order stream (width of 0.7 to 2.5 m - Sabbag & Zina 2011), with continuous canopy height of up to 25 m (P. Dodonov, unpublished data), and a dense savanna classified as cerrado denso, a phytophysiognomy with 50 to 70% of canopy cover and average canopy height of 5 to 8 m (Ribeiro & Walter 1998). We selected seven P. arachnoideum-dominated patches of different areas in this site (Fig. 1a; Tab. 1). Data on ramet density, biomass production and ramet growth in some of these sites were obtained in previous studies (Silva Matos et al. 2014; Xavier et al. 2016, 2019). These patches are characterized by a nearly continuous P. arachnoideum cover; however, they also contain native tree species, albeit with a lower diversity than adjacent non-invaded areas (Fig. 1b-c) (Miatto et al. 2011). Two of the smaller patches included in our study were connected to larger patches. According to managers, before the study period these sites have not been subject to fire or other large disturbances during the last 20 years.

Table 1
Area (in m²) of the six Pteridium arachnoideum-dominated patches along the six-year period. Refer to Figure 1 for the location and shape of the patches.

Patch	Year
	2009	2011	2013	2015
1a	20069	20360	19174	19616
1b	N/A a	1121	1146	1178
2a	6825	6550	7102	7424
2b	NA a	849	762	840
3	1758	0 b	12	0
4	470	802	937	802
5	95	235	200	224

• ^a
  = This patch was not sampled in this year.
• ^b
  = In this year, this patch was occupied by only a few P. arachnoideum ramets.

Data collection

In 2009, 2011, 2013, and 2015, we mapped the contour of each patch (Fig. 1a) with a hand-held GPS device by walking around it as close as possible to the continuous P. arachnoideum cover (Fig. 1b-c), on non-rainy days to minimize the GPS error. Considering the overlap between the cover of this species and of native species, we believe this method to be more precise than the use of satellite imagery, which has been showed to be ineffective for the definition of bracken boundaries (Holland & Aplin 2013); in addition, some of our patches were too small to be detected on satellite images. As we only identified two secondary smaller patches during the second mapping, they were sampled only from 2011 forth.

Data analysis

We used Quantum Gis 2.6 (Quantum Development Team 2013) to create polygons for each patch in each year based on the GPS data and calculated their area. We used mixed-effects linear models to assess temporal trends, including year as fixed variable and patch as random factor, in the lme4 package (Bates et al. 2015). We used log-transformed patch sizes due to non-normality of the residuals with non-transformed data. We performed two analyses, one including all patches and years 2011-2015 and another including all years and only the patches that were measured since 2009. One patch had nearly completely retracted after the first year and was excluded from the analyses; its inclusion, however, did not modify the results. We used Akaike’s information criterion corrected for small sample size (AICc) to compare the adjusted models with null models, which did not contain year but contained patch as random factor, with the bbmle (Bolker & R Development Core Team 2017) package.

Results

Patch dynamics

Maximum patch size was observed in 2009 for one patch, in 2011 for three patches, in 2013 for one patch, and in 2015 for two patches; the smaller patches exhibited a twofold increase from 2009 to 2011, but this increase did not continue over time (Tab. 1; Fig. 1). Conversely, the variation in size of the two larger patches between 2009 and 2015 was of approximately 2% to 9% of their original size in 2009. Some changes in patch shape were observed at the patch borders (Fig. 2). In general, the area occupied by the P. arachnoideum patches was overall stable, with expansion and retraction periods but no clear overall trends (Tab. 1; Fig. 2). However, one patch, where the ramets were apparently subjected to severe herbivory by leafcutter ants (Atta sp.), had occupied 0.17 ha in 2009 but completely retracted by 2015 (Tab. 1; Fig. 2). No temporal trends were observed, as the null model had the lowest AICc in both analyses, with the alternative model having a ∆AICc of 10.8 and 4.4 for the years 2011-2015 and 2009-2015, respectively.

Figure 2
a-b. Size variation of the two largest patches dominated by Pteridium arachnoideum in a savanna-riparian forest transition in the Brazilian southeast. Polygons represent the minimum and maximum size of each patch, corresponding respectively to the years 2013 and 2011 for patch 1a (left) and 2011 and 2015 for patch 2a (right).

Discussion

In this study we showed that undisturbed patches dominated by P. arachnoideum generally remained stable during a six-year period. We only observed little advance and retreat around the patch borders, reflecting an equilibrium state between this species and the surrounding plant community. Similar results were observed in undisturbed patches dominated by P. aquilinum during over 50 years of monitoring (Marrs & Hicks 1986). We believe that this stability is consistent with the response of individual ramets to canopy cover, with increased growth in height under high canopy cover (Xavier et al. 2019), as a greater investment in ramet height under lower light availability is not an adequate strategy to promote vegetative spread under an undisturbed forest canopy. First, P. arachnoideum ramets are unable to achieve enough height to capture light in the upper layer, as the average tree height in our sites is higher than 10 m (Miatto et al. 2011). In addition, because ramets of Pteridium exhibit very low diameter variability (Xavier et al. 2019), very high ramets are more subjected to damage by wind and prostration (Marrs & Watt 2006), which would increase mortality rates and decrease light absorption. Thus, our findings suggest that preventing large disturbances would be the best strategy to avoid the dominance of P. arachnoideum in tropical forest communities.

In addition to low photosynthetic capacity under low light availability, the high mortality of newly emerged ramets may play a role on the size stability of undisturbed P. arachnoideum dominated patches. Xavier et al. (2019) found over 50% of ramet mortality of P. arachnoideum at our study site; in their study, there was nearly no survival where ramets either emerged under canopy with more 75% closure or were subjected to herbivory by leaf cutting ants during the phase of expansion of pinnae, which appears to have contributed to the full retraction of P. arachnoideum in one patch. High ramet mortality in the early stages of development of P. arachnoideum has also been reported for P. aquilinum (Hara et al. 1993). This is surprising because clonal species often exhibit lower mortality rates (Cain 1990; Pennings & Callaway 2000) and higher resilience to herbivory (Schmid et al. 1988; Gao et al. 2013) than non-clonal species during the early development as a result of clonal integration. However, ramet mortality often increases during the transition from the use of rhizome reserves to self-supported primary production, particularly when there is no generation overlap or this is very little (Harper 1977), such as in species of the genus Pteridium (Marrs & Watt 2006). On the one hand, the very high ramet mortality where canopy cover was high (Xavier et al. 2019) suggests that P. arachnoideum ramet survival may be partially dependent on self-supported primary production (Marrs & Watt 2006). On the other hand, considering the potential sharing of defense signals between ramets (Stuefer et al. 2004; Gómez & Stuefer 2006), it is also possible that very low light availability and herbivory are cues to self-induced ramet mortality, as translocating resources to support additional growth of damaged ramets would be less advantageous. Further ecophysiological studies should investigate the relative importance of the photosynthetic rates of bracken ramets to their own survival under multiple environmental conditions. Regardless, our results show that adequate abiotic conditions, especially regarding light incidence, are essential for the expansion of P. arachnoideum into forested areas, which is therefore unlikely to occur in the absence of disturbances.

The retreat of P. arachnoideum associated with plant herbivory was accompanied by an expansion of the African grass Urochloa eminii (Mez) Davidse, which is highly resistant to defoliation (Klink 1994), and then by native shrub species (RO Xavier, personal observation). These changes disagree with our original hypothesis, according to which a six-year period would be too brief for retraction to be detected. However, all other patches remained stable during a period of 6 years, suggesting that in the absence of external factors they will maintain a stable size in the medium term. Gradual retraction of Pteridium and replacement by woody species had been previously reported based on decades of satellite imagery from undisturbed sites of cerrado (Pinheiro & Durigan 2012) and heathlands (Marrs & Watt 2006). These successional changes are more probable to occur after a longer period because they likely depend on both a natural decline in the performance of the clonal species (Marrs & Hicks 1986; de Witte & Stöcklin 2010) and effective seed rain from the surrounding vegetation. Here we only mapped the contour of the Pteridium-dominated patches, while some indications of decline could also be related to lower ramet density and higher density of other species within the patches (Marrs & Hicks 1986). Even though a precise prediction about the future of these sites also depends on monitoring both these characteristics, field excursions carried out in 2009 within the patches indicated that the cover of Pteridium was nearly continuous, suggesting that the patches that remained stable could be effectively in a phase of equilibrium with the surrounding vegetation.

Even though no bracken patch spread during the study period, the presence of smaller patches adjacent to the larger ones highlights the importance of vegetative spread ability for the dispersal of P. arachnoideum. Considering the little distance between these secondary patches, we believe that they resulted from the vegetative spread of larger patches to more suitable sites. This successful spread may be related to foraging ability, which may be defined as the ability to detect better growing conditions in spatially heterogeneous ecosystems, and has been reported for a number of clonal species (De Kroon & Hutchings 1995). Spatial and temporal variation in habitat suitability for ramet growth is expected to occur even in undisturbed riparian forests and dense savannas (MacDougall & Kellman 1992; Lemos-Filho et al. 2010), and effective resource translocation and an extensive underground reserves system may support clonal dispersion in spatially heterogeneous environments (Stuefer et al. 1994; De Kroon et al. 2005). Therefore, our findings are consistent with the prevalence of vegetative spread as a mechanism to small local spread of P. arachnoideum even in undisturbed riparian sites.

In conclusion, we observed stability of patches dominated by Pteridium arachnoideum during a period of 6 years, suggesting that their spread to these forest-savanna transitions is unlikely in the absence of large canopy disturbances. Although high canopy cover and ant herbivory may also constrain the survival of newly emergent ramets and hence the persistence and spread of these patches and although we observed full retraction of one patch, the formation of new patches by means of vegetative growth is likely to ensure long-term persistence of P. arachnoideum. Further studies should investigate strategies to limit the growth and survival of newly emergent ramets, which seems to be the critical phase for the spread of this species. However, our results suggest that under a lack of large canopy disturbances this species is not a threat to the biodiversity of these savanna-riparian forest transitions. Considering that controlling P. arachnoideum to promote forest recovery tends to be expensive and may favour the spread of invasive non-native species (Xavier et al. 2023), our study shows that relying on tree regeneration and a natural decline of clonal patches may be the most appropriate strategy to manage this species in tropical forest sites protected from fire.

Acknowlegements

We are thankful to Mauricio Vancine, for creating the maps of our study sites; and to the FAPESP (Fundação de Amparo a Pesquisa do Estado de São Paulo), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), for the scholarships provided for the first and second authors. We also thank Dr. Pedro Bond Schwartsburd and Dr. Lana Sylvestre, for insightful comments on a previous version of this manuscript.

Data availability statement

In accordance with Open Science communication practices, the authors inform that additional data is available on the first author's Github repository: <https://github.com/pdodonov/publications>.

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Edited by

Area Editor: Dra. Lana Sylvestre

Publication Dates

• Publication in this collection
  01 Dec 2023
• Date of issue
  2023

History

• Received
  28 Mar 2023
• Accepted
  28 Sept 2023