Global Change Biology (2015) 21, 2055–2069, doi: 10.1111/gcb.12820 No evidence that elevated CO2 gives tropical lianas an advantage over tropical trees DAVID C. MARVIN1,4, KLAUS WINTER2 , ROBYN J. BURNHAM1 andSTEFAN A. SCHNITZER2,3 1Department of Ecology and Evolutionary Biology, University of Michigan, 830 N. University Ave., Ann Arbor, MI 48109, USA, 2Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Republic of Panama, 3School of Freshwater Sciences, University of Wisconsin-Milwaukee, P.O. Box 413, Milwaukee, WI 53201, USA Abstract Recent studies indicate that lianas are increasing in size and abundance relative to trees in neotropical forests. As a result, forest dynamics and carbon balance may be altered through liana-induced suppression of tree growth and increases in tree mortality. Increasing atmospheric CO2 is hypothesized to be responsible for the increase in neotropi- cal lianas, yet no study has directly compared the relative response of tropical lianas and trees to elevated CO2.We explicitly tested whether tropical lianas had a larger response to elevated CO2 than co-occurring tropical trees and whether seasonal drought alters the response of either growth form. In two experiments conducted in central Panama, one spanning both wet and dry seasons and one restricted to the dry season, we grew liana (n = 12) and tree = (n 10) species in open-top growth chambers maintained at ambient or twice-ambient CO2 levels. Seedlings of eight individuals (four lianas, four trees) were grown in the ground in each chamber for at least 3 months during each sea- son. We found that both liana and tree seedlings had a significant and positive response to elevated CO2 (in biomass, leaf area, leaf mass per area, and photosynthesis), but that the relative response to elevated CO2 for all variables was not significantly greater for lianas than trees regardless of the season. The lack of differences in the relative response between growth forms does not support the hypothesis that elevated CO2 is responsible for increasing liana size and abundance across the neotropics. Keywords: carbon cycle, global change, mixed-effects models, open-top chambers, Panama, seasonal drought, tropical forests Received 10 September 2014 and accepted 16 October 2014 tree growth, reproduction, and lifespan, combined with Introduction their very low contribution to forest biomass, suggests Lianas (woody vines) are increasing in size and abun- a future in which neotropical forests will absorb and dance relative to trees throughout neotropical forests store less atmospheric carbon dioxide annually (van (Schnitzer & Bongers, 2011; Schnitzer et al., 2012; Yorke der Heijden et al., 2013; Schnitzer et al., 2015). Lianas et al., 2013; Laurance et al., 2014). Reported annual commonly comprise a large proportion of the woody increases in liana abundance range from 0.23% to 7.8% species and stem number in tropical forests (Schnitzer over recent decades, whereas trees either underwent et al., 2012, 2015); however, lianas constitute a small smaller annual increases or have declined in abundance proportion of total tropical forest biomass (Putz, 1983; in the same study areas (Phillips et al., 2002; Chave Gerwing & Farias, 2000; DeWalt & Chave, 2004; Letcher et al., 2008; Enquist & Enquist, 2011; Schnitzer et al., & Chazdon, 2009). Nevertheless, lianas have a dispro- 2012). Liana seedling recruitment, reproduction, and portionately large negative effect on tree biomass accu- leaf productivity have also increased relative to trees mulation by reducing tree diameter increment (Lowe & (Wright et al., 2004; Wright & Calderon, 2006; Benitez- Walker, 1977; Whigham, 1984; Clark & Clark, 1990; Malvido & Martınez-Ramos, 2003). Grauel & Putz, 2004; van der Heijden & Phillips, 2009; The reported increases in liana abundance have Schnitzer et al., 2015), leaf productivity (Dillenburg broad implications for the global carbon cycle because et al., 1993; Perez-Salicrup et al., 2001; Toledo-Aceves & tropical forests account for the single largest terrestrial Swaine, 2008), sap flow velocity (Tobin et al., 2012; Alv- share (60%) of annual global carbon dioxide uptake arez-Cansino et al., in press), and stem height (Perez- (Pan et al., 2011). The negative effect that lianas exert on Salicrup, 2001). Lianas also increase tree mortality (Putz, 1984; Phillips et al., 2002; Garrido-Perez et al., 4Present Address: Department of Global Ecology, Carnegie Insti- 2008; Ingwell et al., 2010; Schnitzer et al., 2015) and sup- tution for Science, 260 Panama St, Stanford, CA 94305, USA press tree regeneration (Toledo-Aceves & Swaine, 2008; Correspondence: David C. Marvin, tel. 860 601 0852, fax 650 462 Schnitzer & Carson, 2010). Depending on the level of 5968, e-mail: [email protected] infestation, lianas are associated with a 1.6–1.9% excess © 2014 John Wiley & Sons Ltd 2055 2056 D. C. MARVIN et al. risk of annual tree mortality (Phillips et al., 2002; Ing- liana species grown under elevated CO2, but found that well et al., 2010). the other measured traits did not show a consistent The causes of increasing lianas have not been empiri- positive response to CO2. Condon et al. (1992) reported cally determined, but the main putative mechanisms that two congeneric species of tropical lianas exposed include increased intensity of seasonal drought, higher to elevated CO2 increased in total biomass, leaf area, € rates of natural and anthropogenic disturbance, and and height compared with ambient CO2.Korner & Ar- increasing atmospheric CO2 (Phillips et al., 2002; Schnit- none (1992) found neither an aboveground biomass zer & Bongers, 2011). Increasing atmospheric CO2 is response nor an increase in leaf area index, but instead often invoked as the primary cause of increasing lianas reported increased root mass under elevated CO2 for (e.g. Phillips et al., 2002) because global atmospheric two liana and three tree species. However, the results € CO2 levels have increased 40% since 1750 (IPCC, 2013), reported by Korner & Arnone (1992) did not compare with well over half the increase occurring since 1960 the responses between the two growth forms. Due to (NOAA, 2013). Because lianas invest less in structural the lack of a direct comparison of lianas and trees to support, relying instead on trees for access to the high- elevated atmospheric CO2 in the tropics, we are cur- light environment of forest canopies, their ratio of leaf rently unable to conclude that lianas respond more area to stem or total plant biomass (LAR) is higher than than trees to increased atmospheric CO2. Moreover, no in trees (Zhu & Cao, 2009, 2010; Paul & Yavitt, 2011). studies have tested the combined effects of elevated The high LAR of lianas may allow them to take advan- CO2 and seasonal drought on the performance of co- tage of increases in CO2 levels to a greater extent than occurring tropical lianas and trees. can trees (Schnitzer & Bongers, 2011). Lianas and trees We tested the hypothesis that lianas respond more have similar photosynthetic capacity per unit leaf area than trees to elevated atmospheric CO2 using a phy- (Asner & Martin, 2012), therefore lianas should gain logenetically diverse set of liana and tree species in proportionally more carbon per unit of plant mass due common gardens in the Republic of Panama. We to their relatively greater leaf area. This additional car- examined the growth of seedlings of twelve liana bon should give lianas an advantage over trees through species and ten tree species grown in the ground greater growth and reproduction, leading to increasing within open-top chambers maintained at either liana density, biomass, and productivity relative to ambient or elevated CO2. We included seasonal trees in tropical forests. drought as a factor and examined the response of Lianas may have a further advantage over trees both growth forms to elevated CO2 over two stud- under elevated atmospheric CO2 in forests that ies: one conducted during the dry season only (‘dry- experience seasonal drought. Liana abundance peaks only’) and one conducted during both wet and dry in highly seasonal tropical forests (Schnitzer, 2005; seasons (‘wet-dry’). Specifically, we tested the DeWalt et al., 2010), apparently because of their abil- hypothesis that relative to ambient CO2: (1) lianas ity to outperform trees during seasonal drought grow more than trees under elevated CO2, and (2) (Schnitzer, 2005; Cai et al., 2009). Elevated CO2 may lianas have an additional growth advantage under increase the water-use efficiency of plants by reduc- elevated CO2 during seasonal drought. ing stomatal conductance and increasing rates of photosynthesis (Battipaglia et al., 2012; Cernusak Materials and methods et al., 2013), thus allowing more carbon to be fixed per unit water lost through transpiration. Seasonal Site and species drought-adapted lianas may increase carbon fixation, and thus water-use efficiency, proportionally more We conducted the study along a forest edge at the Smith- than trees under elevated CO2 because water-stress sonian Tropical Research Institute’s (STRI) Experimental or deciduousness may limit carbon gain in many Outdoor Research Facility at Santa Cruz, Gamboa, in the trees during periods of seasonal drought (Schnitzer Republic of Panama (Fig. 1a). The location was along a & Bongers, 2011). secondary forest edge that was previously cleared for resi- dential housing but never developed, and is now managed To date, just three greenhouse studies of lianas pro- by STRI. Over the past 7 years, STRI has collected hourly vide the evidence for elevated CO2 as an explanation readings of temperature, precipitation, and full-sun photo- – for increasing liana abundance none of which com- synthetically active radiation (PAR) at this site (K. Winter, pared the response of lianas to trees. Given the techni- unpublished data). During the wet season (May–Decem- cal and logistical constraints of working with adult ber), the monthly average daytime temperature is 27.9 °C, lianas and trees, these studies test the CO2 hypothesis average monthly precipitation is 244 mm, and average À at the seedling stage. For example, Granados & Korner€ daily total PAR is 25.2 mol m 2.