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Liana density declined and basal area increased over 12 y in a subtropical montane forest in Argentina

Published online by Cambridge University Press:  21 June 2017

Sergio Javier Ceballos  and
Agustina Malizia
Sergio Javier Ceballos*
Affiliation:
Instituto de Ecología Regional, UNT-CONICET. Casilla de Correo 34. CP. 4107. Yerba Buena, Tucumán, Argentina
Agustina Malizia
Affiliation:
Instituto de Ecología Regional, UNT-CONICET. Casilla de Correo 34. CP. 4107. Yerba Buena, Tucumán, Argentina
*
*Corresponding author. Email: sjc_499@hotmail.com
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Abstract:

Changes in density and basal area of lianas ≥2 cm diameter were monitored in two 1-ha permanent plots in a subtropical montane mature forest of north-western Argentina. Liana stems were identified and measured at 130 cm from the main rooting point in two censuses conducted in 2003 and 2015. Between censuses, the density of liana stems decreased 13.3%, while basal area increased 11.5%. Density and basal area decreased mainly among lianas of 2–3 cm diameter, but increased in lianas ≥4 cm diameter. Quechualia fulta (Asteraceae), Serjania meridionalis (Sapindaceae) and Chamissoa altissima (Amaranthaceae) suffered large reductions in stem density and basal area. Dissimilar responses of density and basal area of lianas might be a consequence of the suppression of anthropogenic disturbances (e.g. livestock browsing) and the decrease of treefall gap frequency in the studied forest in recent decades. Light-demanding liana species decreased and shade-tolerant species increased possibly in response to the decline in the light availability associated with forest recovery from past disturbance. Lianas increased in basal area to a lesser extent compared with reports from several tropical and subtropical forests where lianas are increasing dramatically.

Keywords

basal areadensitydisturbancelianaslight-demanding speciespermanent plotshade-toleranceyungas forests
Type
Research Article
Information
Journal of Tropical Ecology , Volume 33 , Issue 4 , July 2017 , pp. 241 - 248
Copyright
Copyright © Cambridge University Press 2017 

INTRODUCTION

In recent decades, lianas have increased dramatically in abundance and basal area in tropical and subtropical old-growth forests (Campanello et al. Reference CAMPANELLO, VILLAGRA, GARIBALDI, RITTER, ARAUJO and GOLDSTEIN2012, Chave et al. Reference CHAVE, OLIVIER, BONGERS, CHÂTELET, FORGET, VAN DER MEER, NORDEN, RIÉRA and CHARLES-DOMINIQUE2008, Foster et al. Reference FOSTER, TOWNSEND and ZGANJAR2008, Ingwell et al. Reference INGWELL, WRIGHT, BECKLUND, HUBBELL and SCHNITZER2010, Laurance et al. Reference LAURANCE, ANDRADE, MAGRACH, CAMARGO, VALSKO, CAMPBELL, FEARNSIDE, EDWARDS, LOVEJOY and LAURANCE2014, Phillips et al. Reference PHILLIPS, VÁSQUEZ MARTÍNEZ, ARROYO, BAKER, KILLEN, LEWIS, MALHI, MONTEAGUDO MENDOZA, NEILL, NÚÑEZ VARGAS, ALEXIADES, CERÓN, DI FIORE, ERWIN, JARDIM, PALACIOS, SALDIAS and VINCETI2002, Schnitzer & Bongers Reference SCHNITZER and BONGERS2011, Schnitzer et al. Reference SCHNITZER, MANGAN, DALLING, BALDECK, HUBBELL, LEDO, MULLER-LANDAU, TOBIN, AGUILAR, BRASSFIELD, HERNANDEZ, LAO, PEREZ, VALDEZ and YORKE2012, Wright & Calderon Reference WRIGHT and CALDERON2006, Wright et al. Reference WRIGHT, CALDERON, HERNANDEZ and PATON2004, Yorke et al. Reference YORKE, SCHNITZER, MASCARO, LETCHER and CARSON2013). For example, in a 50-ha plot in Barro Colorado Island (Panama), Schnitzer et al. (Reference SCHNITZER, MANGAN, DALLING, BALDECK, HUBBELL, LEDO, MULLER-LANDAU, TOBIN, AGUILAR, BRASSFIELD, HERNANDEZ, LAO, PEREZ, VALDEZ and YORKE2012) observed that over a 30-y period lianas ≥1 cm and ≥5 cm diameter increased in density 75% and 140%, respectively. The opposite trend has also been reported in forests of Africa, where lianas are decreasing in density and basal area (Bongers & Ewango Reference BONGERS, EWANGO, Schnitzer, Bongers, Burnham and Putz2015, Caballé & Martin Reference CABALLÉ and MARTIN2001, Ewango Reference EWANGO2010, Thomas et al. Reference THOMAS, BURNHAM, CHUYONG, KENFACK, SAINGE, Schnitzer, Bongers, Burnham and Putz2015).

Lianas compete intensely with trees for both above- and below-ground resources (Chen et al. Reference CHEN, BONGERS, CAO and CAI2008, Schnitzer et al. Reference SCHNITZER, KUZEE and BONGERS2005), at least partially because they deploy large leaf areas above their host trees (Schnitzer & Bongers Reference SCHNITZER and BONGERS2011). Liana infestation may affect tree recruitment, growth, fecundity and survival (Campanello et al. Reference CAMPANELLO, GARIBALDI, GATTI and GOLDSTEIN2007, Ingwell et al. Reference INGWELL, WRIGHT, BECKLUND, HUBBELL and SCHNITZER2010, Putz Reference PUTZ1984, Schnitzer et al. Reference SCHNITZER, KUZEE and BONGERS2005, Toledo-Aceves & Swaine Reference TOLEDO-ACEVES and SWAINE2008). Therefore, increases in lianas could alter forest dynamics and reduce the ability of a forest to sequester carbon (i.e. lianas may displace far more biomass than they accumulate) (Ingwell et al. Reference INGWELL, WRIGHT, BECKLUND, HUBBELL and SCHNITZER2010, Laurance et al. Reference LAURANCE, ANDRADE, MAGRACH, CAMARGO, VALSKO, CAMPBELL, FEARNSIDE, EDWARDS, LOVEJOY and LAURANCE2014, Schnitzer & Bongers Reference SCHNITZER and BONGERS2011, Schnitzer et al. Reference SCHNITZER, VAN DER HEIJDEN, MASCARO and CARSON2014, van der Heijden & Phillips Reference VAN DER HEIJDEN and PHILLIPS2009, van der Heijden et al. Reference VAN DER HEIJDEN, POWERS and SCHNITZER2015).

Increasing natural and anthropogenic disturbance rates are two of the proposed explanations for liana density increase (Schnitzer Reference SCHNITZER2005, Schnitzer & Bongers Reference SCHNITZER and BONGERS2011). Increasing forest disturbance results in the formation of more edge and gap habitat, where lianas may proliferate (Putz Reference PUTZ1984, Schnitzer et al. Reference SCHNITZER, DALLING and CARSON2000) by using several mechanisms such as seed, advance regeneration (i.e. seedlings and saplings that were present prior to gap formation), lateral growth and long-distance clonal recruitment (Peñalosa Reference PEÑALOSA1984, Schnitzer et al. Reference SCHNITZER, DALLING and CARSON2000). On the other hand, lianas may decrease with decreasing forest disturbances and/or with the ageing of gaps (Malizia & Grau Reference MALIZIA and GRAU2008, Putz Reference PUTZ1984).

Most lianas species are pioneers or light-demanding due to their high abundance in disturbed and well-illuminated areas, such as treefall gaps, young secondary stands and forest edges (DeWalt et al. Reference DEWALT, SCHNITZER and DENSLOW2000, Londré & Schnitzer Reference LONDRÉ and SCHNITZER2006, Putz Reference PUTZ1984). However, this does not mean that all liana species are shade-intolerant (Gianoli et al. Reference GIANOLI, SALDAÑA, JIMÉNEZ-CASTILLO and VALLADARES2010), and in fact they appear to show different shade-tolerance levels (Gilbert et al. Reference GILBERT, WRIGHT, MULLER-LANDAU, KITAJIMA and HERNANDEZ2006). It has been suggested that with the increase of disturbances, light-demanding liana species might benefit (Roeder et al. Reference ROEDER, HÖLSCHER and KOSSMANN-FERRAZ2012), while shade-tolerant species may decrease. In addition, a density increase of shade-tolerant species is expected when a decrease in disturbance occurs and the forest understorey becomes darker.

In a mature subtropical montane forest of Sierra de San Javier (Tucuman, Argentina), we monitored lianas ≥2 cm diameter over a 12-y period (2003–2015), to assess how liana density and basal area changed between the two censuses. The hypotheses are: (1) Lianas are common in well-illuminated environments and tend to decrease in density and basal area probably due to the reduction of light availability associated to the forest recovery from past disturbances (DeWalt et al. Reference DEWALT, SCHNITZER and DENSLOW2000, Ewango Reference EWANGO2010). Thus, we expected that lianas became less abundant in respond to the anthropogenic disturbance suppression in the forest since the area was included in a natural reserve in 1973. (2) We expected the greatest decrease in density for light-demanding species due to the decline in light availability.

STUDY SITE

This study was conducted in a subtropical montane mature forest located at ~1000 m asl in Parque Sierra de San Javier (26°45′S, 65°20′W), a 14,000-ha protected area, 10 km west of San Miguel de Tucuman, Argentina. The area represents the southern-most extension of the Andean montane forests, also known as yungas (Cabrera & Willink Reference CABRERA and WILLINK1980). The vegetation corresponds to a semideciduous forest, with an average of 23 tree species ha−1 ≥10 cm diameter (Grau Reference GRAU2002, Malizia & Grau Reference MALIZIA and GRAU2006) and canopy heights of 15–30 m dominated by shade-tolerant species such as Blepharocalyx salicifolius (Myrtaceae), Ocotea porphyria (Lauraceae) and Pisonia zapallo (Nyctaginaceae). The subcanopy (5–12 m) is dominated by Eugenia uniflora (Myrtaceae), Piper tucumanum (Piperaceae) and Allophylus edulis (Sapindaceae), while the shrub Psychotria carthaginensis (Rubiaceae) forms a relatively uniform layer in the understorey (Grau Reference GRAU2002, Malizia & Grau Reference MALIZIA and GRAU2006, Malizia et al. Reference MALIZIA, EASDALE and GRAU2013). The forest includes 11 species ha−1 of liana ≥2 cm diameter (Malizia et al. Reference MALIZIA, GRAU and LICHSTEIN2010), and the most abundant species are Cissus striata (Vitaceae), Chamissoa altissima (Amaranthaceae) and Celtis iguanaea (Celtidaceae), which together represent c. 60% of the individuals (Malizia & Grau Reference MALIZIA and GRAU2006). This mature forest had signs of minor recent human influence. It was selectively logged c. 50 y ago (i.e. only two cut stumps were recorded in a 6-ha permanent plot when established in 1992) and subjected to livestock browsing up to 1973 when Parque Sierra de San Javier was created (Grau Reference GRAU2002, Grau & Brown Reference GRAU, BROWN, Dallmaier and Comiskey1998, Malizia et al. Reference MALIZIA, EASDALE and GRAU2013).

The study area receives ~1300–1600 mm of rainfall annually and has a seasonal monsoonal climate (Bianchi & Yáñez Reference BIANCHI and YÁÑEZ1992). Mean annual temperature is 18.8°C (Bianchi & Yáñez Reference BIANCHI and YÁÑEZ1992), but temperatures drop to −5°C about once per decade (Torres Bruchmann Reference TORRES BRUCHMANN1978).

METHODS

Sampling

In 1992, a 6-ha permanent plot was established in the study area in order to monitor tree demography and gap dynamics over time (Easdale et al. Reference EASDALE, HEALEY, GRAU and MALIZIA2007, Grau Reference GRAU2002, Malizia et al. Reference MALIZIA, EASDALE and GRAU2013), and was extended in 2003 to include lianas (Malizia Reference MALIZIA2007). The 6-ha plot is part of a larger forest monitoring system of the Instituto de Ecología Regional (IER, Universidad Nacional de Tucumán – CONICET) and consists of a 300 × 200 m rectangle, divided in 150 20 × 20 m quadrats (400 m2) in which all trees ≥10 cm diameter at breast height (dbh) are permanently marked, measured, mapped, identified and re-measured (or recorded as dead) every 5 y (Grau Reference GRAU2002, Malizia et al. Reference MALIZIA, EASDALE and GRAU2013). In 2003, climbing lianas with stem diameters ≥2 cm were identified, measured at 130 cm from the main rooting point, painted with non-toxic paint, marked with aluminium tags and mapped in a xy coordinate system over the 6-ha plot (Malizia & Grau Reference MALIZIA and GRAU2006). A diameter of 2 cm was considered as a threshold since lianas of this size have approximately as much leaf mass as a 10-cm-diameter tree, the common minimum threshold for trees to be considered in a measurement (Gerwing & Farias Reference GERWING and FARIAS2000). When an individual liana had multiple stems, an aluminium tag was attached to the largest diameter stem and nails to the others (Malizia & Grau Reference MALIZIA and GRAU2006). Lianas were re-measured during 2015 following the protocol of Gerwing et al. (Reference GERWING, SCHNITZER, BURNHAM, BONGERS, CHAVE, DEWALT, EWANGO, FOSTER, KENFACK, MARTÍNEZ-RAMOS, PARREN, PARTHASARATHY, PÉREZ-SALICRUP, PUTZ and THOMAS2006), in two 1-ha plots within the 6-ha permanent plot, providing a re-measurement period of 12-y. New liana recruits ≥2 cm dbh were identified, measured in diameter, painted and permanently marked with numbered aluminium tags.

In liana ecology, studies usually define apparent genets, comprised of one or more ramets that are visibly connected (Gerwing et al. Reference GERWING, SCHNITZER, BURNHAM, BONGERS, CHAVE, DEWALT, EWANGO, FOSTER, KENFACK, MARTÍNEZ-RAMOS, PARREN, PARTHASARATHY, PÉREZ-SALICRUP, PUTZ and THOMAS2006, Schnitzer et al. Reference SCHNITZER, MANGAN, HUBBELL, Schnitzer, Bongers, Burnham and Putz2015). In our study, we distinguished apparent genets (hereafter individuals) from liana ramets (hereafter stems) but only through observation of stems connections on or above the soil surface. Stems that were physically attached to another stem were considered part of the same individual, while those not visibly connected were considered separate individuals.

Data analysis

The data collected in the 2015 census were compared with data of the 2003 census to describe changes in liana density and basal area over the 12 y, at plot, species and diameter-size-class levels. These changes were not analysed with statistical tests due to the unreplicated plot design.

To analyse the relationship between liana species density change and their different shade-tolerance levels, we first obtained a continuum axis of shade-tolerant species using a Principal Component Analysis (PCA). This ordination method was chosen to obtain a shade-tolerance gradient of liana species using different proxy variables such as growth and mortality rates (Condit et al. Reference CONDIT, ASHTON, BUNYAVEJCHEWIN, DATTARAJA, DAVIES, ESUFALI, EWANGO, FOSTER, GUNATILLEKE, GUNATILLEKE, HALL, HARMS, HART, HERNANDEZ, HUBBELL, ITOH, KIRATIPRAYOON, LAFRANKIE, DE LAO, MAKANA, NOOR, KASSIM, RUSSO, SUKUMAR, SAMPER, SURESH, TAN, THOMAS, VALENCIA, VALLEJO, VILLA and ZILLIO2006), wood density, seed size and the abundance distribution in two contrasting light environments (we sampled young and mature forests in the Sierra de San Javier to represent high and low light conditions, respectively). The reduction of the number of variables into a single synthetic variable (i.e. the first component of the PCA) was considered a useful approach to differentiate shade-tolerant and light-demanding species. However, our approach focused on a gradient of species with different tolerance to shade rather than two distinct groups (i.e. shade-tolerant vs. light-demanding species). The main matrix for this analysis contained liana species in rows and the variables mentioned above in columns. Variables were analysed through PCA correlation matrix and were standardized by the standard deviation before running the analysis due to their different units. First two axes comprised 68.6% of the cumulative variance, but we selected only the first axis that explained 45.5% to interpret the results. Then, we performed a linear regression analysis between species scores on the shade-tolerance axis (PCA1) and changes in their density in the 2003–2015 period (considered as change in percentage between censuses). The variable change in density per species was standardized into a range of 0 to 1 with the ‘decostand’ function in the ‘vegan’ package and transformed to logarithm (X + 1) to reduce the variability among species and to fulfil the normality requirement. Shade-tolerance scores were also standardized into a range of positive values from 0 to 1 to remove negative PCA values. All analyses were performed with the statistical program R (R Development Core Team).

RESULTS

In 2015, we surveyed a total of 929 liana stems and 775 liana individuals belonging to 12 species and nine families that range from 2 to 13 cm and have a mean size of 4.3 cm in two 1-ha plots. The most abundant species in 2015 were Cissus striata (286 stems and 242 individuals), Celtis iguanaea (156 stems and 124 individuals) and Chamissoa altissima (119 stems and 94 individuals). The mean density of lianas ≥2 cm diameter in each quadrat (400 m2) was 19 stems (range = 2–35) and 16 individuals (range = 2–32). Species richness was similar between 2003 and 2015 (11 and 12 species, respectively), but in the 2015 census, one species was not recorded (Muehlenbeckia sagittifolia – Polygonaceae) and two were added (Cissus verticillata – Vitaceae and Gonolobus rostratus – Apocynaceae).

Between 2003 and 2015, the density of lianas stems ≥2 cm diameter decreased from 536 ha−1 to 465 ha−1 (−13.3%), and the density of liana individuals decreased similarly, from 439 ha−1 to 388 ha−1 (−11.7%). The density of lianas of 2–3 cm diameter decreased (−54%), but increased in the ≥4 cm diameter classes (+57%; Figure 1). Quechualia fulta and Serjania meridionalis showed a large reduction in stem density by 65% and 37%, respectively (Table 1). Basal area increased from 0.69 to 0.78 m2 ha−1 (+11.5%) between censuses. There were differences in basal area change among diameter size classes, decreasing for lianas of 2–3 cm (−55%), but increasing for lianas ≥4 cm (+53%; Figure 1). Most species increased in basal area, while only S. meridionalis (−29%), Q. fulta (−22%), and C. altissima (−20%) declined (Table 1).

Figure 1. Density (a) and basal area (b) of lianas in 2003 and 2015 by size class recorded at Sierra de San Javier, Tucuman, Argentina. Black and white bars represent liana density per census and error bars represent 1 SD.

Table 1. Changes in density (stems ha−1) and basal area (m2 ha−1) between 2003 and 2015 for liana species of two 1-ha plots of Sierra de San Javier, Tucuman, Argentina

We obtained a shade-tolerance axis, based on the correlations of wood density, growth, mortality and abundance in young vs. mature forests with axis 1 of the PCA (hereafter referred to as shade-tolerance axis; Figure 2, Table 2). With decreasing scores in shade-tolerance axis, species exhibit higher wood density, lower growth, lower mortality and greater abundance in shaded areas (in mature forests). With increasing scores in axis two, species exhibit larger seeds. Species with higher scores in the shade-tolerance axis (light-demanding) showed the highest decrease in density, while those with lower scores (shade-tolerant) increased (R2 = 0.41, F = 5.4, P = 0.04; Figure 3).

Figure 2. Ordination diagram (PCA) used to identify a shade-tolerance axis among liana species, defined by demographic and functional variables (Appendix 1). Variables are represented by vectors and species by labels: AT (Acacia tucumanensis), CA (Chamissoa altissima), CI (Celtis iguanaea), CS (Cissus striata), DU (Dolichandra unguis-cati), HO (Hebanthe occidentalis), HD (Heteropterys dumetorum), PA (Pisoniella arborescens), QF (Quechualia fulta), and SM (Serjania meridionalis).

Table 2. Correlations between variables and PCA axes.

Figure 3. Linear regression between the shade-tolerance axis and change in species density over a 12-y period (2003–2015) at Sierra de San Javier, Tucuman, Argentina. The shade tolerance increases towards lower scores in x-axis. Change in species density was logarithmically transformed. Each species is represented by a black circle.

DISCUSSION

Over a 12-y period, lianas showed dissimilar responses in density and basal area in two 1-ha plots of mature forest at Sierra de San Javier. The decrease occurred mainly in small-sized lianas (2–3 cm diameter), which have high density and a major influence on total density change. Basal area increased annually 0.96 m2 ha−1 in the plots but at lower levels than the reports of other tropical and subtropical forests (e.g. an annual increase of 3.72 m2 ha−1 in Amazonian sites; Phillips et al. Reference PHILLIPS, VÁSQUEZ MARTÍNEZ, ARROYO, BAKER, KILLEN, LEWIS, MALHI, MONTEAGUDO MENDOZA, NEILL, NÚÑEZ VARGAS, ALEXIADES, CERÓN, DI FIORE, ERWIN, JARDIM, PALACIOS, SALDIAS and VINCETI2002), and occurred mainly due to the density increase of higher-size lianas (≥4 cm diameter).

The mature forest of the study area exhibited changes in tree structure in the last two decades (Grau et al. Reference GRAU, PAOLINI, MALIZIA, CARILLA and Grau2010, Malizia et al. Reference MALIZIA, EASDALE and GRAU2013). Plots established in this forest had a 54% increase in tree stem density and 6% in tree basal area between 1992 and 2007, which have been mainly attributed to forest recovery of palatable tree species (i.e. nutrient-rich soft-leaved species) after the removal of livestock (Malizia et al. Reference MALIZIA, EASDALE and GRAU2013). Anthropogenic disturbances (e.g. livestock browsing) decreased when the area was included in a natural reserve in 1973 (Grau et al. Reference GRAU, HERNÁNDEZ, GUTIERREZ, GASPARRI, CASAVECCHIA, FLORES and PAOLINI2008) and probably influenced liana density decrease within the studied forest, as suggested for lianas in other forests of the world (Bongers & Ewango Reference BONGERS, EWANGO, Schnitzer, Bongers, Burnham and Putz2015, Ewango Reference EWANGO2010, Pandian & Parthasarathy Reference PANDIAN and PARTHASARATHY2016). For example, lianas are also decreasing in forests that are recovering from past disturbances in Ituri region (Democratic Republic of Congo) (Bongers & Ewango Reference BONGERS, EWANGO, Schnitzer, Bongers, Burnham and Putz2015, Ewango Reference EWANGO2010). Also, in tropical forests of India, Pandian & Parthasarathy (Reference PANDIAN and PARTHASARATHY2016) observed that increases in liana density between 2003–2013 were positively correlated with the increase of different local disturbances. These observations support the notion of Schnitzer & Bongers (Reference SCHNITZER and BONGERS2011), which suggest that changes in liana abundance may be a more local than continental phenomenon, with lianas increasing in some areas (Chave et al. Reference CHAVE, OLIVIER, BONGERS, CHÂTELET, FORGET, VAN DER MEER, NORDEN, RIÉRA and CHARLES-DOMINIQUE2008, Ingwell et al. Reference INGWELL, WRIGHT, BECKLUND, HUBBELL and SCHNITZER2010, Laurance et al. Reference LAURANCE, ANDRADE, MAGRACH, CAMARGO, VALSKO, CAMPBELL, FEARNSIDE, EDWARDS, LOVEJOY and LAURANCE2014, Phillips et al. Reference PHILLIPS, VÁSQUEZ MARTÍNEZ, ARROYO, BAKER, KILLEN, LEWIS, MALHI, MONTEAGUDO MENDOZA, NEILL, NÚÑEZ VARGAS, ALEXIADES, CERÓN, DI FIORE, ERWIN, JARDIM, PALACIOS, SALDIAS and VINCETI2002, Schnitzer et al. Reference SCHNITZER, MANGAN, DALLING, BALDECK, HUBBELL, LEDO, MULLER-LANDAU, TOBIN, AGUILAR, BRASSFIELD, HERNANDEZ, LAO, PEREZ, VALDEZ and YORKE2012) and decreasing or remaining stable in others (Bongers & Ewango Reference BONGERS, EWANGO, Schnitzer, Bongers, Burnham and Putz2015, Caballé & Martin Reference CABALLÉ and MARTIN2001, Ewango Reference EWANGO2010, Londré & Schnitzer Reference LONDRÉ and SCHNITZER2006, Thomas et al. Reference THOMAS, BURNHAM, CHUYONG, KENFACK, SAINGE, Schnitzer, Bongers, Burnham and Putz2015).

The decrease in the density of gaps within the plots may be another mechanism that explains liana structural and compositional changes. Gaps caused by fallen stems ≥50 cm diameter (monitored every 5 y within the plots using different techniques; Grau Reference GRAU2002) exhibited a maximum density in the 1982–1992 period (i.e. 8–12 gaps ha−1) and a drastic reduction afterwards (i.e. 1–2 gaps ha−1 recorded between 2002 and 2012). The factor controlling the change in gap frequency in this forest remains unknown, but might be related to climate (e.g. the rise in the number of gaps was during the 1980s when precipitations increased; H.R. Grau pers. obs.). Consequently, light availability decreased within the forest influencing lianas, which usually decline in density when canopy closes (Malizia & Grau Reference MALIZIA and GRAU2008, Putz Reference PUTZ1984). Light-demanding liana species showed the larger decrease in density while shade-tolerant species increased, probably in response to the shade conditions created when gaps closed. In addition, some of these species, such as Q. fulta and C. altissima are scramblers (Malizia & Grau Reference MALIZIA and GRAU2008), lianas that are common on gaps and low-canopy areas and tend to decrease as the canopy increases its height (Hegarty & Caballé Reference HEGARTY, CABALLÉ, Putz and Mooney1991, Putz & Holbrook Reference PUTZ, HOLBROOK, Putz and Mooney1991).

Liana species of this study were distributed along a continuous gradient of shade-tolerance, suggesting that only a few species can be strictly classified as shade-tolerant or shade-intolerant. This notion is supported by Putz (Reference PUTZ1984), in which from over 65 species from Barro Colorado Island (Panama), only three were classified as gap-phase or early successional and only two as shade-tolerants. Like trees, liana species appear to vary in their tolerance to shade (Gilbert et al. Reference GILBERT, WRIGHT, MULLER-LANDAU, KITAJIMA and HERNANDEZ2006) and this pattern is related to the trade-off between high survival and rapid growth (Cai et al. Reference CAI, POORTER, CAO and BONGERS2007, Ewango Reference EWANGO2010, Gerwing Reference GERWING2004, Gilbert et al. Reference GILBERT, WRIGHT, MULLER-LANDAU, KITAJIMA and HERNANDEZ2006), which reflects the resource allocation to survival-enhancing traits (Kitajima Reference KITAJIMA1994). In addition to this trade-off, we noted that liana species with high survival and low diameter growth possessed higher wood density, which was not previously reported for lianas to our knowledge.

Shade tolerance is an important trait that has been scarcely taken into account for lianas, despite its relevance to species response to forest succession and disturbances (i.e. processes that change light environment in forests). It has been suggested that adaptation to light exploitation of liana species explains their abundance across a disturbance-mediated light gradient (Gianoli et al. Reference GIANOLI, SALDAÑA, JIMÉNEZ-CASTILLO and VALLADARES2010, Mori et al. Reference MORI, KAMIJO and MASAKI2016). Consequently, we may predict that light-demanding species will benefit from increasing disturbance, while shade-tolerant species will benefit in forests recovering from past disturbance. This prediction can be supported by the higher decrease in density and basal area of light-demanding species found in this study (e.g. Q. fulta, S. meridionalis and C. altissima) and in DR Congo (e.g. Manniophytom fulvum), probably in response to a reduction in forest disturbance (Ewango Reference EWANGO2010). Additionally in a temperate forest, the shade-tolerant liana Euonymus fortunei could increase its abundance under the current lack of large and intensive disturbances (Mori et al. Reference MORI, KAMIJO and MASAKI2016). However, more studies are necessary to improve our knowledge of the strategies of liana species that are changing in density in different forests of the world.

CONCLUSION

The density and basal area of lianas showed dissimilar changes over a 12-y period in a mature forest of Sierra de San Javier. Even though density decreased, basal area increased but at lower levels than reported in other tropical and subtropical forests where lianas are becoming more dominant. Light-demanding liana species decreased while shade-tolerant species increased in density. We suggest that these changes are controlled by the reduction in both natural (treefall gap frequency) and anthropogenic disturbances (livestock browsing) in recent decades, which may influence liana density due to their close relation with forest disturbance dynamics. We recommend that density change of species with different shade-tolerance should be assessed in long-term monitoring of lianas, due to its relevance in front of the current increase of disturbances and forest recovery processes in several regions.

ACKNOWLEDGEMENTS

We thank José Tisone and Ivan Jerez for field assistance; Instituto de Ecología Regional (IER) for allowing us to work in their forest monitoring system; Francis E. Putz at the Department of Biology of the University of Florida for providing me with an office and facilities for data analysis; Sofía Nanni for the help with the English version of this manuscript. This research was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and by Cooperación Internacional UF-CONICET (526/15).

Appendix 1. Growth, mortality, recruitment, wood density, seed size and abundance of the 10 most common liana species of two 1-ha plots of Sierra de San Javier, Tucuman, Argentina. N is the number of stems used to calculate mean growth rate per species. The range of growth per species between 2003 and 2015 is indicated in parentheses. Abundance has two classes: 1 (species more abundant in mature forests) and 2 (species abundant in both young and mature forest). No species was more abundant in young forests.

References

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Figure 0

Figure 1. Density (a) and basal area (b) of lianas in 2003 and 2015 by size class recorded at Sierra de San Javier, Tucuman, Argentina. Black and white bars represent liana density per census and error bars represent 1 SD.

Figure 1

Table 1. Changes in density (stems ha−1) and basal area (m2 ha−1) between 2003 and 2015 for liana species of two 1-ha plots of Sierra de San Javier, Tucuman, Argentina

Figure 2

Figure 2. Ordination diagram (PCA) used to identify a shade-tolerance axis among liana species, defined by demographic and functional variables (Appendix 1). Variables are represented by vectors and species by labels: AT (Acacia tucumanensis), CA (Chamissoa altissima), CI (Celtis iguanaea), CS (Cissus striata), DU (Dolichandra unguis-cati), HO (Hebanthe occidentalis), HD (Heteropterys dumetorum), PA (Pisoniella arborescens), QF (Quechualia fulta), and SM (Serjania meridionalis).

Figure 3

Table 2. Correlations between variables and PCA axes.

Figure 4

Figure 3. Linear regression between the shade-tolerance axis and change in species density over a 12-y period (2003–2015) at Sierra de San Javier, Tucuman, Argentina. The shade tolerance increases towards lower scores in x-axis. Change in species density was logarithmically transformed. Each species is represented by a black circle.

Figure 5

Appendix 1. Growth, mortality, recruitment, wood density, seed size and abundance of the 10 most common liana species of two 1-ha plots of Sierra de San Javier, Tucuman, Argentina. N is the number of stems used to calculate mean growth rate per species. The range of growth per species between 2003 and 2015 is indicated in parentheses. Abundance has two classes: 1 (species more abundant in mature forests) and 2 (species abundant in both young and mature forest). No species was more abundant in young forests.