Ficus Spp.) in a Tropical Cloud Forest: Evaluation of a Potential Keystone Resource

Journal of Tropical Ecology (2013) 29:401–407. © Cambridge University Press 2013 doi:10.1017/S0266467413000461

Phenology, abundance and consumers of ﬁgs (Ficus spp.) in a tropical cloud forest: evaluation of a potential keystone resource

Gustavo H. Kattan∗,†,1 and Leonor A. Valenzuela∗,‡

∗ Fundacion´ EcoAndina, Carrera 2 A Oeste No. 12-111, Cali, Colombia † Departamento de Ciencias Naturales y Matematicas,´ Pontificia Universidad Javeriana Cali, Avenida Canasgordas˜ No. 118-250, Cali, Colombia ‡ Departamento de Ecolog´ıa, Pontificia Universidad Catolica´ de Chile and Instituto de Ecolog´ıa y Biodiversidad (IEB), Santiago, Chile (Received 21 January 2013; revised 21 June 2013; accepted 22 June 2013; first published online 26 July 2013)

Abstract: Fig trees (Ficus spp) produce fruit year-round and figs are consumed by a large proportion of frugivores throughout the tropics. Figs are potential keystone resources that sustain frugivore communities during periods of scarcity, but studies have produced contradictory results. Over 1 y we monitored the phenology of 206 trees of five Ficus species in a Colombian cloud forest, to test whether figs produced fruit during periods of low overall fruit availability. We also measured fig tree densities in 18 0.5-ha plots and made 190 h of observations at 24 trees of three species to determine whether figs were abundant and consumed by a large proportion of the local frugivores. The five species produced fruit year-round but fig availability varied monthly by orders of magnitude. Fig trees reached comparatively high densities of 1–5 trees ha−1 and were consumed by 36 bird species (60% of the local frugivore assemblage) and three mammal species. However, there was no season of fruit scarcity and figs represented on average 1.5% of the monthly fruit biomass. Figs in this Andean forest are part of a broad array of fruiting species and at least during our study did not seem to constitute a keystone resource.

Key Words: cloud forest, Colombia, Ficus, frugivory, keystone resource, phenology, tree density

INTRODUCTION which, with few exceptions, is species-specific (Cook & Rasplus 2003). Female wasps emerging from a tree need The fruits of fig trees (Ficus spp., Moraceae) are to find another tree in a short time, with syconia in the an important food source for fruit-eating vertebrates appropriate stage for colonization. Thus, syconium pro- throughout the tropics and subtropics. Globally, over duction within a tree is synchronous but among trees it is 1200 species of bird and mammal (>10% of the world’s asychronous. Fruit production of figs is usually abundant, birds and >6% of mammals) are known to feed on figs and trees of different species at a particular locality initiate and Ficus is considered the most important plant genus syconium production at different times, resulting in fruit for tropical frugivores (Shanahan et al. 2001). Locally, being available every month of the year (Milton 1991, Ficus is usually the most diverse genus and always ranks Ragusa-Netto 2002, Tweheyo & Lye 2003). among the top 10 most diverse genera in lowland tropical The abundance and constancy of fig availability forests (Harrison 2005). Figs are consumed by up to 45% year-round support the proposition that these trees of the local bird and mammal faunas (Shanahan et al. are keystone resources for the frugivore community of 2001). Figs also represent a critical resource for particular tropical forests. The role of figs as a keystone resource groups of species such as Asian hornbills (Bucerotidae), by has been supported by work in Malaysia (Lambert & providing a large proportion of their diet and influencing Marshall 1991), India (Kannan & James 1999), South their grouping and ranging patterns (Kinnaird & O’Brien Africa (Bleher et al. 2003) and Panama (Korine et al. 2005, Kinnaird et al. 1996). 2000). However, for various reasons that include low The importance of fig trees hinges on their capacity fig densities and not providing sufficient resources during to produce fruit throughout the year. Fig pollination periods of scarcity, other studies have not found support depends on a specialized relationship with agaonid wasps for the keystone role of figs in localities in Gabon (Gautier- Hion & Michaloud 1989), Uganda (Chapman et al. 2005), 1 Corresponding author. Email: [email protected] India (Patel 1997) and Colombia (Stevenson 2005).

Downloaded from https:/www.cambridge.org/core. Pontificia Universidad Catolica de Chile, on 11 Jan 2017 at 18:36:59, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. http://dx.doi.org/10.1017/S0266467413000461 402 GUSTAVO H. KATTAN AND LEONOR A. VALENZUELA

Peres (2000) proposed that a keystone resource should meet the following criteria: (1) exhibit low redundancy, i.e. be available during periods of overall fruit scarcity, (2) be consumed by a large percentage of the frugivore community, (3) exhibit interannual reliability, and (4) be abundant.Inthispaperwedescribethefigtreeassemblage of a cloud forest in the tropical Andes of Colombia to evaluate its potential role as a keystone plant resource. Over 1 y, we followed the phenology of five species of fig tree and quantified fruit production in comparison with overall fruit production in the forest, to test the hypothesis that figs provided abundant food during periods when other fruits were scarce. We also estimated fig tree density and surveyed bird and diurnal mammal consumers to determine whether fig trees at this site met the criteria of being abundant and consumed by a large proportion of local frugivores. Our study lasted only 1 y so we cannot test the criterion of interannual reliability, but we can Figure 1. Precipitation regime at El Cedral meteorological station, 2000 determine whether during our study figs were a keystone masl,6kmeastoftheOtun´ Quimbaya Flora and Fauna Sanctuary, central range of the Colombian Andes. The graph shows mean and SD resource. for 30 y.

the herbarium of Universidad del Valle (CUVC) in Cali, STUDY AREA Colombia. The study was conducted at Otun´ Quimbaya Flora and To test for temporal differences in number of individuals Fauna Sanctuary, a 411-ha protected area on the western in fruit, number of fruits and dry biomass, we used a χ 2 slope of the central range of the Andes of Colombia, near test, with the mean value for the 12 mo as the the city of Pereira. Otun´ Quimbaya spans altitudes of expected value. We tested for asynchrony in the inter- 1800–2000 m asl and is adjacent to Ucumar´ıRegional tree phenological patterns with the evenness index H (Bronstein & Patel 1992), Park, another protected area of 4000 ha encompassing altitudes between 1700 and 2600 m asl. The area is 5 = − − 0.2 covered with humid, montane cloud forest in a mosaic H 1 Pi 1.6 of mature forest and secondary regeneration of different i=1 ages between 10 and 60 y old. Annual precipitation is where Pi is the proportion of trees with syconia in the 2650 mm, with two peaks of rainfall in April and October five phases of development. The index varies between 0 and relatively drier seasons in December–January and and 1 and a value of 1 indicates an even distribution, i.e. July–August (Aguilar & Rangel 1994; Figure 1). asynchrony. To estimate fig tree density we marked and counted fig trees in 0.5-ha plots (N = 18). Between December 2003 METHODS and September 2004 we conducted 190 h of observation of bird and mammal consumers in 24 focal trees of three We collected data along 14 trails of variable length. species of Ficus (F. andicola, F. killipii and F. mutisii; Each fig tree within 8 to 22 m of either side of the Table 1). The number of trees monitored varied between trails (depending on visibility) was marked and located one and six per month. For each tree, we made between on a map of the study area. Phenology was monitored three and eight observation sessions between 06h00 and monthly between November 2003 and November 2004. 10h00. For each bird and mammal visitor, we noted the We recognized five phases of syconium development: pre- species and counted the number of consumption events. A female, female, interfloral, male and postfloral (mature consumption event was defined as an individual arriving syconia). We estimated crop size by counting the number at the tree and feeding on fruits, independently of the of fruits on a visible branch and extrapolating to the number of figs eaten. entire tree. We collected 50 fruits from different trees To determine whether Ficus spp. were fruiting during (dependingonhowmanytreesfruited)foreachfigspecies, periods of fruit scarcity, we used community-wide and obtained dry mass by drying fruits in an oven until phenological data obtained in a parallel study over constant mass. We also measured their height and width. the same time period (M. Kessler-Rios & G. Kattan, Voucher specimens of the five species were deposited at unpubl. data). Monthly estimates of fruit production were

Table 1. Ficus species recorded at the study site, Otun´ Quimbaya Flora and Fauna Sanctuary, Central Andes of Colombia. Taxonomic order according to www.figweb.org/Ficus/Classification_of_figs. For each species, the table shows median crop size (with range and sample size in parentheses), the total number of trees monitored (N), fig dimensions based on 50 syconia of each species, and mean tree density ± SD obtained from 0.5-ha plots (N = 18). Ficus species Crop size N Mean fig dimensions (mm) Mean fig mass (g) Density (trees ha−1) Subgenus Pharmacosycea F. mutisii Dugand 1620 (210–3460; 8) 31 11 × 9 0.3 2.8 ± 3.2 Subgenus Urostigma F. andicola Standl. 1736 (18–24 320; 53) 111 8 × 8 0.2 3.2 ± 3.9 F. hartwegii (Miq.) Miq. 4680 (880–14400; 6) 19 19 × 18 0.4 5.0 ± 6.7 F. killipi Standl. 14 230 (120–1 416 960; 11) 35 6 × 5 0.1 2.2 ± 4.3 F. aff. cuatrecasana Dugand 11 450 (220–24 480; 3) 11 28 × 24 0.9 1.0 ± 1.8

obtained from all trees and shrubs with dbh >2.5 cm in The evenness index showed a high degree of 15 transects (50 × 4 m) in the same habitats. For each asynchrony among all individuals in the five species in plant in fruit, the number of fruits on a visible branch was flowering/fruiting periods. Indices varied between 0.68 counted or estimated and this number was extrapolated in November 2004 and 0.99 in July. For the most to the entire plant. Samples of fruit pulp of all plants abundant species in our sample of fruiting trees, F. were dried until constant mass and weighed. From these andicola, asynchrony was also high (index values between data we extrapolated to the entire crop to obtain monthly 0.63 and 0.99). Within trees, in contrast, synchrony in estimatesofdrybiomassproduction.Forspecieswithlarge fruit production was very high (LV pers. obs.). Densities seeds (e.g. Lauraceae, Arecaceae), we removed the seeds of the five tree species varied between 1 and 5 trees ha−1 and dried the pulp but for some species with watery fruits (Table 1). and very small seeds (e.g. Melastomataceae), the seeds We observed 36 species of bird feeding on figs of were not removed. three species (F. andicola, F. killipii and F. mutisii). A subgroup of 14 bird species were recorded in six or more months. These species included several tanagers (Tangara RESULTS spp.), black-billed thrush (Turdus ignobilis), Swainson’s thrush (Catharus ustulatus) and emerald toucanet The five fig tree species produced fruit during the year (Aulacorhynchus prasinus). Two species of squirrel (Sciurus of study. There was great variation among species in granatensis and Microsciurus sp.) and red howler monkey crop and syconium size (Table 1). During the year of (Alouatta seniculus) also fed on figs, although the howler observation, 81 out of 206 trees (39.3%) presented monkey did not feed on the small fruits of F. andicola. syconia in at least one of the five development phases. Between December 2004 and September 2005 we Thirteen trees aborted their syconia after the female recorded between 12 and 19 consumer species every phase, and our study ended before three additional trees month in the 24 fig trees that we monitored. reached the ripe fruit phase. Therefore, we have complete Werecordedatotalof1521consumptionevents,which cycles for 65 trees. varied monthly between 3.2 and 24.7 events h−1,with Fruit availability (ripe syconia) varied throughout the an increase between June and September (Figure 3). The year. There was variation in the monthly number of trees most common consumers were different in the three fig χ 2 = = presenting ripe fruits ( 11 3.9, P 0.04), with a low of species. In F. andicola the black-billed thrush represented one individual in August and September and a high of 10 34% of consumption events, whereas in F. killipii the individuals in March (Figure 2). most common consumer was the Cauca guan (Penelope There was significant variation among months in the perspicax) with 29% of consumption events and in χ 2 = < numberoffruits( 11 31.6, P 0.001). Mean fruit F. mutisii, the emerald toucanet with 32%. availabilitywas145,000±396,000fruitsmo−1 (range= Community-wide fruit production varied between 30 20–1.5 million; Figure 2). There also was significant and 50 species and between 60 and 120 individuals in χ 2 = < monthly variation in fruit biomass ( 11 19.3, P fruit every month (understorey and canopy combined). 0.001; Figure 2). The median of monthly biomass was Fruit availability of Ficus, measured as dry biomass 238 g ha−1 and varied between 0.2 and 3300 g ha−1. (g ha−1) represented a fraction of the total fruit biomass in The low number of individuals in fruit in August and the forest that varied between 0 and 8% (mean = 1.5%; September was reflected in very low biomass availability Figure 3). The highest fraction occurred in March 2004, in those months. Biomass in March was very high because whenthreefigtreesproducedmassivecrops.Therewasno of the massive fruiting of three large trees (two F. mutisii correlation between fig biomass and overall fruit biomass and one F. killipii). (r = 0.28, P = 0.35, N = 12).

Figure 2. Fig availability at a cloud-forest site in the Andes of Colombia, between November 2003 and November 2004. Graphs show the number of individual fruiting trees per month for ﬁve species of Ficus, with precipitation for the year of study (a), the total number of ﬁgs (log-transformed) (b), and total dry biomass for trees fruiting in 14 transects (c).

DISCUSSION by bats; Korine et al. 2000) but we sampled a relatively small area of the 411-ha reserve and only in late second- In our study site in Andean cloud forest, fig-tree fruiting growth and mature forest, so we may have missed some was inter- and intraspecifically asynchronous and the species. Ficus is usually a very diverse genus in tropical five species of fig produced fruit throughout the year. forests. For example, 35 species are known for Cocha This corroborates previous findings that figs provide a Cashu (1000 ha) in Peru and 16 for La Selva (1500 permanent, although in this case highly variable, food ha) in Costa Rica (Harrison 2005). The small number supply for frugivorous birds and mammals. of fig species found in our study may be an effect of We found only five species of fig (and an additional area, altitude or habitat heterogeneity. We are not aware four species of green-fruited fig that are usually consumed of any studies that have analysed altitudinal trends in

Figure 3. Dry fruit biomass of ﬁve species of red-fruited Ficus compared with total fruit biomass in a cloud forest in the central range of the Colombian Andes, November 2003 to November 2004. The graph also shows consumption rates (events h−1) by birds and mammals in three Ficus spp.

Ficus species richness, but the genus is highly diverse (Giraldo et al. 2007). In addition, figs may be important ecologically and occupies a diversity of niches (Harrison sources of specific nutrients such as calcium (O’Brien 2005). Therefore, expanding our study to include more et al. 1998). Therefore, figs indeed represent an important area and other habitat types (e.g. valleys, forest edges, resource for the frugivore community in this cloud forest. early second-growth) will probably reveal more species. However, there was no season of scarcity during our Fig tree densities, in contrast, are high in our study study and figs represented a small fraction of the total area, compared with lowland rain-forest sites. The five fruit available in the area. species had densities of >1 individual ha−1, whereas in The fruits of over 200 species of tree and shrub in localities throughout the tropics densities vary between this Andean forest are consumed by birds and diurnal 0.01 and 0.9 individuals ha−1 (Harrison 2005). A study mammals (Rios et al. 2004), and plants such as Cecropia in southern India also reported relatively high densities telealba and Melastomataceae also provide abundant, of 11 trees ha−1 in an open trail and 5.6 trees ha−1 in year-round food sources that are eaten by a large primary forest (Athreya 1999). The high Ficus density at proportion of the local frugivores, particularly tanagers our site may reflect density compensation related to the (Kessler-Rios & Kattan 2012, Rios 2005). Some species lower species diversity of montane forest. of Melastomataceae, such as Miconia acuminifera, which The 36 species of bird that we recorded consuming is consumed by tanagers and the howler monkey, may figs in this study represent 60% of the 60 species in reach densities of 220 trees ha−1 (Giraldo et al. 2007, the area that regularly or occasionally include fruits Kessler-Rios & Kattan 2012). in their diets (GHK, unpubl. data). More extensive Fig availability was highly variable in time and space. monitoring will likely add more species to the list of fig Out of 206 trees that we monitored, 125 did not initiate consumers. Consumption rates of figs were two to five syconium production during the year of observation. times higher than rates reported for several species of Although fig trees are abundant, at any given time only Melastomataceae, another food resource important for a small proportion of trees are in fruit and these are tropical frugivorous birds and consumed by the same widely scattered. A keystone resource should be abundant bird species at our site (Kessler-Rios & Kattan 2012). Our enough to sustain the local community of frugivores observations suggest that some species such as tanagers (Stevenson 2005). In addition to the criteria proposed by and red howler monkey seem to rely heavily on figs. Peres (2000), determining whether a particular resource A previous study at the same site also identified figs as is a keystone, should also consider the spatial scale of its important components in the diet of the howler monkey availability (location of fruiting trees at any particular

time) in relation to the patterns of movement and habitat ATHREYA, V. R. 1999. Light or presence of host trees: which is more use of its consumers. Some frugivores move over large important for the strangler fig? Journal of Tropical Ecology 15:589– spatial scales, but scattered fruiting trees may be out of 603. reach for many frugivores that move over small scales BLEHER, B., POTGIETER, C. J., JOHNSON, D. N. & BOHNING-GAESE,¨ K. (Duran´ & Kattan 2005, Garc´ıa & Ortiz-Pulido 2004, 2003. The importance of figs for frugivores in a South African coastal Kinnaird et al. 1996). The variance in fig availability was forest. Journal of Tropical Ecology 19:375–386. very high in our study, which is likely a result of the BRONSTEIN, J. L. & PATEL, A. 1992. Causes and consequences of relatively small spatial scale of our observations. Variance within-tree phenological patterns in the Florida strangling fig, Ficus in fruit availability could be expected to decrease with aurea (Moracea). American Journal of Botany 79:41–48. increasing spatial scale, but it remains to be determined CHAPMAN, C. A., CHAPMAN, L. J., ZANNE, A. E., POULSEN, J. R. whether the scale at which this variance is minimized & CLARK, C. J. 2005. A 12-year phenological record of fruiting: coincides with the scale of movements of most frugivores. implications for frugivore populations and indicators of climate Existing studies suggest that northern Andean wet change. Pp. 75–92 in Dew, J. L. & Boubli, J. P. (eds). Tropical fruits and forests do not usually exhibit seasons of generalized frugivores: the search for strong interactors. Springer, Dordrecht. fruit scarcity as occurs in lowland rain forest, although COOK, J. M. & RASPLUS, J. Y. 2003. Mutualists with attitude: coevolving localized scarcities and supra-annual cycles of fruit fig wasps and figs. Trends in Ecology and Evolution 18:241–248. availability may occur (Ataroff 2001, Giraldo 1990, DURAN,´ S. M. & KATTAN, G. H. 2005. A test of the utility of exotic tree Giraldo et al. 2007). In our study area, a drop in plantations for understory birds and food resources in the Colombian fruit availability usually occurs between September and Andes. Biotropica 37:129–135. December, but the magnitude of the drop is variable and GARCÍA, D. & ORTIZ-PULIDO, R. 2004. Patterns of resource tracking a period of relative scarcity may occur in some years by avian frugivores at multiple spatial scales: two case studies on (Munoz˜ et al. 2007; M. Kessler-Rios & G. Kattan, unpubl. discordance among scales. Ecography 27:187–196. data). Therefore, if the Ficus fruiting pattern holds among GAUTIER-HION, A. & MICHALOUD, G. 1989. Are figs always keystone years, then figs may be a fallback food for some species resources for tropical frugivorous vertebrates? A test in Gabon. in some years, but during the year of our study fruit was Ecology 70:1826–1833. abundant and figs did not constitute a keystone resource. GIRALDO, J. 1990. Estudio fenologico´ de una comunidad vegetal en We conclude that most of the time figs are part, albeit an un bosque montano humedo´ en la cordillera Occidental. Cespedesia important one, of a broad array of fruiting species (Rios 16:53–75. et al. 2004) in this Andean forest. GIRALDO, P., GOMEZ-POSADA,´ C., MARTÍNEZ, J. & KATTAN, G. 2007. Resource use and seed dispersal by red howler monkeys (Alouatta seniculus) in a Colombian Andean forest. Neotropical Primates 14:55– 64. ACKNOWLEDGEMENTS HARRISON, R. D. 2005. Figs and the diversity of tropical rainforests. BioScience 55:1053–1064. We thank the National Parks Unit and the staff at the KANNAN, R. & JAMES, D. A. 1999. Fruiting phenology and the Otun´ Quimbaya Flora and Fauna Sanctuary for permits conservation of the great pied hornbill (Buceros bicornis)inthe and logistical support. For help with field work we thank western Ghats of southern India. Biotropica 31:167–177. Y. Toro, W. Cardona and P. Giraldo. Thanks to M. Kessler- KESSLER-RIOS, M. M. & KATTAN, G. H. 2012. Fruits of Rios for sharing phenology data. The study was funded Melastomataceae: phenology in Andean forest and role as a food by a grant from the John D. and Catherine T. MacArthur resource for birds. JournalofTropicalEcology28:11–21. Foundation through the Wildlife Conservation Society. KINNAIRD, M. F. & O´BRIEN, T. G. 2005. Fast foods of the forest: the WethankRhettHarrisonandthreeanonymousreviewers influence of figs on primates and hornbills across Wallace’s line. Pp. for comments that improved the paper. 155–184inDew,J.L.&Boubli,J.P.(eds.).Tropicalfruitsandfrugivores: the search for strong interactors. Springer, Dordrecht. KINNAIRD, M. F., O’BRIEN, T. G. & SURYADI, S. 1996. Population fluctuation in Sulawesi red-knobbed hornbills: tracking figs in space LITERATURE CITED and time. Auk 113:431–440. KORINE, C., KALKO, E. K. V. & HERRE, E. A. 2000. Fruit characteristics AGUILAR, M. & RANGEL, J. O. 1994. Clima del Parque Regional and factors affecting fruit removal in a Panamanian community of Natural Ucumar´ı y sectores aledanos.˜ Pp. 39–57 in Rangel, J. O. strangler figs. Oecologia 123:560–568. (ed.). Ucumar´ı: un caso t´ıpico de la diversidad biotica´ andina. Corporacion´ LAMBERT, F. R. & MARSHALL, A. G. 1991. Keystone characteristics Autonoma´ Regional de Risaralda, Pereira, Colombia. of bird-dispersed Ficus in a Malaysian lowland rain forest. Journal of ATAROFF, M. 2001. Venezuela. Pp. 397–442 in Kapelle, M. & Brown, Ecology 79:793–809. A. (eds). Bosques nublados del Neotropico´ . Instituto Nacional de MILTON, K. 1991. Leaf change and fruit production in six neotropical Biodiversidad, Santo Domingo de Heredia, Costa Rica. Moraceae species. Journal of Ecology 79:1–26.

MUNOZ,˜ M. C., LONDONO,˜ G. A., RIOS, M. M. & KATTAN, G. H. 2007. RIOS, M. M. 2005. ¿Quien´ come yarumo . . . o mejor, ¿quien´ no come Diet of the Cauca guan: exploitation of a novel food source in times of yarumo en los bosques de montana?˜ Bolet´ın SAO 15:5–15. scarcity. Condor 109:841–851. RIOS, M. M., GIRALDO, P. & CORREA, D. 2004. Gu´ıa de frutos y semillas O’BRIEN, T. G., KINNAIRD, M. F., DIERENFELD, E. S., CONKLIN- de la cuenca media del r´ıo Otun´ . Fundacion´ EcoAndina & Wildlife BRITTAIN, N. L., WRANGHAM, R. W. & SILVER, S. C. 1998. What’s Conservation Society, Cali, Colombia. 248 pp. so special about ﬁgs? Nature 392:668. SHANAHAN, M., SO, S., COMPTON, S. G. & CORLETT, R. 2001. Fig- PATEL, A. 1997. Phenological patterns of Ficus in relation to other eating by vertebrate frugivores: a global review. Biological Reviews forest trees in southern India. Journal of Tropical Ecology 13:681– 76:529–572. 695. STEVENSON, P. 2005. Potential keystone plant species for the frugivore PERES, C. A. 2000. Identifying keystone plant resources in tropical community at Tinigua Park, Colombia. Pp. 37–58 in Dew, J. L. & forests: the case of gums from Parkia pods. Journal of Tropical Ecology Boubli, J. P. (eds). Tropical fruits and frugivores: the search for strong 16:287–317. interactors. Springer, Dordrecht. RAGUSA-NETTO, J. 2002. Fruiting phenology and consumption by TWEHEYO, M. & LYE, K. A. 2003. Phenology of ﬁgs in Budongo Forest birds in Ficus calyptroceras (Miq.) Miq. (Moraceae). Brazilian Journal Uganda and its importance for the chimpanzee diet. African Journal of of Biology 62:339–346. Ecology 41:306–316.