884 ARTICLE

Population dynamics of lambertii in southern Brazilian forest–grassland mosaics Alison Paulo Bernardi, Miguel Busarello Lauterjung, Tiago Montagna, Rafael Candido-Ribeiro, Marcia Patricia Hoeltgebaum, Adelar Mantovani, and Maurício Sedrez dos Reis

Abstract: The grasslands conversion to forests is occurring globally and modifying the population dynamics of species. Here, we characterized the population dynamics of Podocarpus lambertii Klotzsch ex Endl. over four years in southern Brazilian forest– grassland mosaics. We asked (i) if the studied P. lambertii population would decrease or increase over time and (ii) what the role of forest patches is in the growth and recruitment of a P. lambertii population. Thus, we studied forest–grassland mosaics, stratified the population into four demographic classes, evaluated the population dynamics, and estimated the correlation between canopy cover and average number of individuals. All individuals of P. Lambertii occurred in forest patches. Density was high but decreased from seedlings to the reproductive stage. The population growth rate was ␭ = 1.025, and the recruitment of individuals was high and variable among years. The transition and mortality rates showed a pattern of reduction from seedlings to the reproductive stage. Mortality rate for seedlings and juveniles was low and concentrated at the smaller heights. The correlations between canopy cover and the average number of individuals were positive and significant. The ecological charac- teristics of this species and specific conditions provided by forest patches allow population growth and species conservation in the southern Brazilian forest–grassland mosaics.

Key words: canopy cover, , forest patches, matrix population model, invasion of grasslands. Résumé : La conversion des prairies en forêts se poursuit globalement et modifie la dynamique de population des espèces. Dans cet article, nous avons caractérisé la dynamique de population de Podocarpus lambertii Klotzsch ex Endl. sur une période de quatre ans dans les mosaïques de forêt et de prairie du sud du Brésil. Nous nous demandons (i) si la population de P. lambertii à l’étude diminue ou augmente avec le temps et (ii) quel rôle jouent les parcelles de forêt dans la croissance et le recrutement de la population de P. lambertii. Nous avons donc étudié les mosaïques de forêt et de prairie, stratifié la population en quatre classes démographiques, évalué la dynamique de population et estimé la corrélation entre l’étendue du couvert forestier et le nombre moyen d’individus. Tous les individus de l’espèce ont été retrouvés à l’intérieur des parcelles de forêt. La densité était élevée mais diminuait du stade de semis au stade de reproduction. Le taux de croissance de la population était ␭ = 1,025 et le recrutement des

For personal use only. individus était élevé et variable selon les années. Les taux de transition et de mortalité diminuaient du stade de semis au stade de reproduction. Le taux de mortalité chez les semis et les individus du stade juvénile était faible et la mortalité était concentrée parmi les tiges les moins hautes. Les corrélations entre l’étendue du couvert forestier et le nombre moyen d’individus étaient positives et significatives. Les caractéristiques écologiques de cette espèce et les conditions spécifiques associées aux parcelles de forêt permettent la croissance de la population et la conservation de l’espèce dans les mosaïques de forêt et de prairie du sud du Brésil. [Traduit par la Rédaction]

Mots-clés : étendue du couvert forestier, conifères, parcelles de forêt, modèle matriciel de population, invasion des prairies.

Introduction dynamics, and their effects vary from one cohort to another The structure of populations may be shaped by local biotic within a population (Lindström and Kokko 2002). These factors and abiotic conditions and can be characterized in terms of age, may determine different recruitment and mortality rates, espe- size, and form of the individuals that comprise it (Hutchings 1997). cially in the younger classes (e.g., seedlings and juveniles), but also Recruitment, mortality, immigrants, and emigrants determine fecundity rates for later ontogenetic stages (Payo-Payo et al. 2016). the number of individuals in a population and allow one to make Recruitment, mortality, and fecundity rates of can be inferences about the population dynamics of plants through time assessed using population matrix models (PMMs). PMMs were in- troduced with the idea of projecting a structured population size

Can. J. For. Res. Downloaded from www.nrcresearchpress.com by Mr. Alison Paulo Bernardi on 06/18/19 (Hutchings 1997). Environmental conditions (e.g., availability of soil nutrients, moisture, and light), as well as intra- and inter- (age-based models) in distinct steps into the future (Lewis 1942), specific interactions and anthropogenic processes (e.g., logging, but they can also provide a way for calculating population param- livestock management, and fire), are associated with population eters (Leslie 1945). Lefkovitch (1965) extended the use of PMMs by

Received 12 December 2018. Accepted 20 March 2019. A.P. Bernardi, M.B. Lauterjung, T. Montagna, M.P. Hoeltgebaum, and M.S. dos Reis. Núcleo de Pesquisas em Florestas Tropicais, Pós-Graduação em Recursos Genéticos Vegetais, Departamento de Fitotecnia, Centro de Ciências Agrárias, Universidade Federal de Santa Catarina. Rodovia Admar Gonzaga, Florianópolis, Santa Catarina, Brazil. R. Candido-Ribeiro. Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, BC, Canada. A. Mantovani. Uso e Conservação dos Recursos Florestais, Departamento de Engenharia Florestal, Centro de Ciências Agroveterinárias, Universidade do Estado de Santa Catarina, Avenida Luís de Camões, Lages, Santa Catarina, Brazil. Corresponding author: Alison Paulo Bernardi (email: [email protected]). Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink.

Can. J. For. Res. 49: 884–891 (2019) dx.doi.org/10.1139/cjfr-2018-0531 Published at www.nrcresearchpress.com/cjfr on 18 June 2019. Bernardi et al. 885

adding the idea of grouping individuals into classes (stage- mosaics. We asked (i) if the studied P. lambertii population would structured models). In addition, PMMs allow one to categorize a decrease, increase, or remain stable over time and (ii) what the role of population into different stages, sizes, or classes, and individuals forest patches is in the growth and recruitment of P. lambertii can move ahead, stay in the same class, grow, reproduce, or re- population. gress a stage in each time interval (Lefkovitch 1965; Caswell 2001). The use of PMMs in population dynamics studies is not recent (see Materials and methods Ogden (1985) and Zuidema and Zagt (2000)), and it has been ap- Study species plied from different perspectives (Crone et al. 2011, 2013). It is a Podocarpus lambertii naturally occurs in two disjunct areas, one powerful and useful method for assessing population status and in northern Bahia state (11°32.82=S, 41°9.16=W) and another be- extinction risk and planning management and conservation strat- tween Minas Gerais and southern Rio Grande do Sul states egies of plants (Caswell 2001; Crone et al. 2011, 2013). Stage- (29°27.32=S, 54°26.26=W) (Carvalho 2004). It is a dioecious species structured PMMs are especially valuable for long-lived species, because pollinated by bees (Carvalho 2004) and wind (personal observa- population trends of these species (e.g., Araucaria cunninghamii tion, 2017). The seeds are dispersed by animals, mainly birds that Aiton ex D. Don, Araucaria hunsteinii K.Schum., Araucaria angustifolia feed on their fleshy basal receptacles (Kuniyoshi 1983). Podocarpus (Bertol.) Kuntze, Nothofagus fusca (Hook.f.) Oerst., and Pinus palustris lambertii trees may reach up to 27 m in height and 1.2 m in diam- Mill.) are difficult to define throughout their life-span (Zuidema and eter (Carvalho 2004); it is a long-lived species, a heliophyte in its Zagt 2000; Dillingham et al. 2016). In addition, only a few studies early stages of development, but shade-tolerant in later stages have reported PMMs on the genus Podocarpus (Ogden 1985). (Inoue et al. 1984; Longhi et al. 2010). In the understory layer, it Podocarpus lambertii Klotzsch ex Endl. is a long-lived tree species occurs in association with A. angustifolia and in small groups with native to Brazil (Inoue et al. 1984; Carvalho 2004). It occurs in the a high density of individuals (Inoue et al. 1984; Longhi et al. 2010). forest–grassland mosaic and the Araucaria Forest, two different The species has been recognized as valuable for forest planting, ecosystems found in the Pampa and Atlantic Rainforest biomes in restoration of degraded areas (Reitz et al. 1983), and ornamental southern Brazil (Overbeck et al. 2007). Paleoecological data sug- use; however, owing to the negative impact caused by anthropo- ϳ gest that until the Late Holocene ( 4300 years BP), southern Brazil genic processes in its areas of natural occurrence and intensive was almost only grasslands (treeless) owing to climatic conditions timber exploitation in the past, this species is classified as endan- (Behling et al. 2004); however, during the second period of the gered by local (CONSEMA 2014) and international (Farjon 2013) ϳ Late Holocene ( 1100 years BP to present day), the grasslands were lists of threatened species. partially converted into forest patches and a net of gallery forests as a result of climatic oscillations and a marked expansion of Study area elements of the Araucaria Forest (Behling et al. 2004, 2009). The The study area is located in a forest–grassland mosaic in southern process of grassland conversion to forests (e.g., forest–grassland Brazil, in the municipality of Lages, Santa Catarina state, Brazil mosaic) has global importance (Scholes and Archer 1997; Halpern (Fig. 1). The area has forest patches dominated mainly by the co- et al. 2010; Rice et al. 2012), with major consequences in commu- nifers A. angustifolia and P. lambertii. The average elevation of the nity structure and species composition (Scholes and Archer 1997). study area is 1033 m a.s.l., and the climate is classified as Cfb in the Several extrinsic factors such as climate changes, fire, grazing, Köppen System (temperate highland climate with dry winters; and the introduction of livestock (Scholes and Archer 1997; Haugo Kottek et al. 2006). Araucaria angustifolia is an economically, eco- and Halpern 2007) contributed to grassland conversion to forests; For personal use only. logically, and culturally important tree species of the Araucaria however, they were not always beneficial, depending on intensity Forest (Reis et al. 2014, Adan et al. 2016). This species has ecological and frequency of occurrence (Archer et al. 1988; Scholes and characteristics (e.g., dioecious, long-lived pioneer) and a natural Archer 1997). Also, forest species differ in life histories and phys- area of occurrence similar to that of P. lambertii, and it also bene- iological traits and have different abilities to respond to or medi- fits from forest patches. Furthermore, it has been widely studied, ate extrinsic factors (Haugo and Halpern 2010; Halpern et al. 2010). which, in many cases, accounts for its use in taxonomic compar- In addition, intrinsic factors (biotic interactions) should be con- isons. sidered, as they can maintain or accelerate grassland conversion In the study area, no evidence points to selective logging of to forests (Rice et al. 2012). Biotic interactions are fundamental to timber species or fire over the last 40 and 20 years, respectively. grassland conversion to forests, mainly when climate or other Currently, cattle grazing and mowing were observed within part factors inhibit the recruitment and establishment of species of the study area. (Halpern et al. 2010). Southern Brazilian forest–grassland mosaics have been main- Data collection and analysis tained historically by extrinsic factors (Behling et al. 2009). Also, A large, square plot (9 ha, 300 × 300 m) was established within recent and accelerated anthropogenic processes (e.g., agricultural the study site to capture an open area with forest patches within expansion and monoculture forest plantation) have modified and it where P. lambertii occurs (see Fig. 1). We identified and mapped reduced the forest–grassland mosaic areas (Overbeck et al. 2007; all individuals of P. lambertii with height ≥0.1 m occurring inside

Can. J. For. Res. Downloaded from www.nrcresearchpress.com by Mr. Alison Paulo Bernardi on 06/18/19 Behling et al. 2009). The remnants of forest patches are extremely the plot using Cartesian coordinates (x and y, in meters). Life important in this scenario, as they harbor a diversity of tree spe- status (survival and mortality), increment (height and diameter at cies, some of which can modify their environments (e.g., micro- breast height (dbh)), and density were evaluated annually from habitat, soil moisture, light, and competitive herbaceous species) 2013 to 2016. The population was stratified into four demographic favoring initial establishment and growth of other species (see classes: (1) seedling (SE), individuals with height ≥0.1 m and ≤0.5 m; Halpern et al. (2010) and Rice et al. (2012) and references therein), (2) juvenile (JV), individuals with height >0.5 m and ≤1.5 m; (3) imma- as occurs with Araucaria angustifolia, which is considered a nurse ture (IM), individuals with height >1.5 m but without reproductive plant (Duarte et al. 2006; Korndörfer et al. 2014). Moreover, forest structures, and (4) reproductive (RP), male and female individuals patches are responsible for connecting species and maintaining with height >1.5 m and reproductive structures present. All new species diversity through gene flow of seeds and pollen (Duarte individuals reported between 2013 and 2016 were considered re- et al. 2006; Boldrini 2009). cruits. SE and JV classes were evaluated in a central plot of 2.56 ha In this context, the present study aimed to characterize the (160 × 160 m) within the bigger total plot (Fig. 1, study area B), and population dynamics of Podocarpus lambertii over the course of IM and RP classes were evaluated within the boundaries of the four years in the context of southern Brazilian forest–grassland larger plot (Fig. 1, study area A).

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Fig. 1. Map of the study area located in a forest–grassland mosaic in Lages, Santa Catarina state, Brazil. The square plot (A) shows the bigger plot of 9 ha (300 × 300 m) where individuals of immature (IM) and reproductive (RP) classes were evaluated; (B) a smaller plot of 2.56 ha (160 × 160 m) where individuals of seedlings (SE) and juvenile (JV) classes were evaluated. Araucaria forest and grassland domains are based on the vegetation map of South America proposed by Hueck and Seibert (1981).

To address the study questions, we estimated the total number (D) was estimated for each class as follows: D =1–S – G. Fecundity

For personal use only. of individuals and their densities per hectare, as well as the aver- was estimated based on the number of recruits found in the cen- age height and dbh for each class and their respective increments. tral plot between 2013 and 2016, divided by the number of RP For each class, the number of individuals and density were calcu- individuals found inside the same central plot, and multiplied by lated annually; average height and dbh were calculated once us- the probability of remaining in the same RP class for each assessed ing all records throughout the years (2013–2016); and increment year (Caswell 2001). was calculated using only individuals surveyed in all four years Population growth rate was estimated using PMM lambda (␭), (2013–2016), subtracting the first measure (2013) from the last considering the average Lefkovitch matrix (three matrices) and (2016), and dividing the result by the time period (four years). The confidence intervals for current annual increment were con- based on the dominant eigenvalue of the matrix. We constructed ␭ structed using standard error (t test). confidence intervals (95% probability) for the estimate ( ) using We estimated the population growth rate using the Lefkovitch the percentile method with bootstrap resampling (Caswell 2001). population matrix model (PMM), which assumes that an individ- The percentile method was computed by randomly selecting ob- ual of a determined class can die, remain in the same class, or served transitions (S, D,orG) through the analyzed years, fixing grow and reproduce at every time interval, with fixed probabili- individual frequency in each class as the average number of indi- ties for each class (Caswell 2001). Other assumptions of this model viduals in the study period (Maloney 2011). All analyses were per- are that each class can be biologically justified and differs from formed using the popbio package (Stubben and Milligan 2007)in the other classes; all individuals behave in the same way within R(R Core Team 2015). Can. J. For. Res. Downloaded from www.nrcresearchpress.com by Mr. Alison Paulo Bernardi on 06/18/19 each class (same rates of remaining within the same class (S), We estimated canopy cover with a spherical crown densitome- transitioning to the next class (G), mortality (D), and fecundity); ter, convex model A (Lemmon 1956). In each subplot (10 × 10 m), we rates remain constant over time; the population is in a stable stage performed four measurements, one for each point (north, south, distribution; and environmental changes over time are disre- garded (Caswell 2001). east, and west). The sum of these values was multiplied by 1.04 and The probabilities of S, G, and D were all calculated using ob- divided by four (average of the points), representing the canopy served data and class criteria for each year. From these probabil- cover. The correlation between canopy cover and average number ities, three matrices were parameterized, one for each annual of individuals in the SE, JV, and IM classes during the study period transition between 2013 and 2016 (Supplementary Table S11). The was estimated by Spearman correlation using R software (R Core average of these matrices (three) generated the transition matrix Team 2015). All values of canopy cover were transformed by the used for the analysis (Fig. 4; see Paludo et al. 2016). Mortality rate arcsine function.

1Supplementary material (Table S1) is available with the article through the journal Web site at http://nrcresearchpress.com/doi/suppl/10.1139/cjfr-2018-0531.

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Fig. 2. Density by classes and years of individuals of a Podocarpus Discussion lambertii population from Lages, Santa Catarina state, Brazil. Seedling (SE) and juvenile (JV) classes were evaluated in a plot Population growth, recruitment, and mortality measuring 2.56 ha (2013–2016); immature (IM) and reproductive (RP) Historically, selective logging of timber species and fire events classes were evaluated in a plot measuring 9 ha (2013–2016). have occurred in the forest–grassland mosaics, and recently, cat- tle grazing and mowing have occurred in parts of the study area. Nevertheless, the occurrence of P. lambertii individuals in all classes (by height and dbh) shows that the population does not present a gap of individuals in any class. Indeed, the lambda value was significantly positive (␭ = 1.025), and all demographic classes increased over time (Fig. 2), presenting a distribution of individu- als similar to an inverse J-shape, the typical pattern of autogen- erative populations. Other long-lived species also presented population growth increase (␭ > 1), e.g., A. cunninghamii, N. fusca, and P. palustris (Zuidema and Zagt 2000), A. laubenfelsii (Rigg et al. 2010), and A. muelleri (Enright et al. 2013). On the other hand, a population of A. angustifolia studied in an old-growth forest frag- ment tended towards a very slow decline (␭ = 0.997, not signifi- cantly different from 1) as a result of low recruitment and transition between classes in numbers insufficient to compensate for the high mortality rates (Paludo et al. 2016). We found lower density of individuals than Manfredi (2014), who studied three P. lambertii populations located in southern Brazil in areas with forest–grassland mosaics (Bom Jardim da Results Serra, 2653 individuals·ha−1; Lages, 1737 individuals·ha−1; and São José do Cerrito, 3596 individuals·ha−1). In particular, Manfredi Population structure and dynamics (2014) used a distinct methodological approach (e.g., sampled Within the four-year evaluation period, the P. lambertii popula- area) and evaluated individuals shorter than 0.1 m in height, in- tion showed a higher number of individuals in SE and JV classes fluencing the density of individuals. Nevertheless, our density of than in IM and RP classes, presenting an inverse J-shaped distribu- individuals was higher than reported for the same species in rem- tion (Fig. 2). The total density in each year was 738 individuals·ha−1 nants of the Araucaria Forest. The species was found in forest (2013), 887 individuals·ha−1 (2014), 958 individuals·ha−1 (2015), and remnants in the advanced stage of succession and at elevations up 1013 individuals·ha−1 (2016). The density of individuals increased to 1200 m (5.29 individuals·ha−1; n = 14 sample plots), in the me- for SE and JV classes and remained constant for IM and RP classes dium successional stage and at elevations up to 1200 m −1 over the years (Fig. 2). (6.42 individuals·ha ; n = 7), at an elevation above 1200 m −1 The average height of SE, JV, IM, and RP classes was 0.25, 0.82, 4, (15.95 individuals·ha ; n = 4), and overall in a Mixed Ombrophi- −1 and 7.6 m, respectively (Figs. 3A, 3B, 3C, 3D). The current annual lous Forest (MOF; 7.3 individuals·ha ; n = 402) (Meyer et al. 2012).

For personal use only. In addition, we found higher density of individuals than that increment in height was 0.02 m·year−1 (95% CI, ±0.0004; n = 728) observed for P. drouyniaunus (Chalwell and Ladd 2005), P. totara for SE and 0.06 m·year−1 (95% CI, 0.0011; n = 623) for JV. The average (Miller and Wells 2003), and A. angustifolia (Paludo et al. 2016, dbh was 4.5 cm for IM and 15.4 cm for RP (Figs. 3E, 3F). The current −1 Paludo et al. 2011). annual increment in dbh was 0.14 cm·year (95% CI, ±0.0064; n = One factor that influences the number of individuals and re- −1 362) for IM and 0.22 cm·year (95% CI, ±0.0096; n = 314) for RP. cruitment is seed production over the years. Seed production, The average Lefkovitch matrix (Fig. 4) summarizes the P. lambertii consumption, and dispersal are poorly understood in P. lambertii. population dynamics (Supplementary Table S11). The number of Regeneration and recruitment in a population can be limited individuals that remained within the same class (S) increased when seeds are consumed by humans (Reis et al. 2014; Adan et al. from SE to RP, with 83.7% of individuals from the SE class remain- 2016) and (or) wild animals (Vieira and Iob 2009) or when a species ing within the same class, 94% remaining in the JV class, 97.3% presents variation in seed production (Mantovani et al. 2004), as remaining in the IM class, and 99.5% remaining in the RP class. occurs in A. angustifolia. However, in our study, regeneration and The transition to the next successive class (G) and mortality rate (D) recruitment do not seem to be limited as no evidence points to presented a pattern of reduction from SE to RP. The mortality human consumption of the fleshy basal receptacles, despite being rates (D) for classes SE and JV were concentrated in the smaller edible, and seed production can be considered high, as indirectly heights (0.1–0.2 m; Fig. 5B) and showed values of 9.1% and 2%, determined through annual recruitment. In addition, P. lambertii respectively. IM and RP classes presented lower D, with values of has high annual survival rates in all classes, even for the SE class Can. J. For. Res. Downloaded from www.nrcresearchpress.com by Mr. Alison Paulo Bernardi on 06/18/19 2% and 0.5%, respectively. (SE = 0.909), which would normally exhibit low survival rates The recruitment of individuals was variable among all years. In (<45%) compared with adult individuals (Paludo et al. 2016; Moustakas and Evans 2015; Rigg et al. 2010). the first year (2013–2014), 491 individuals were recorded; in the Other factors may influence mortality rate. In our study, D was second year (2014–2015), 338 individuals were recorded; and in the low, decreasing from SE to RP, and it was concentrated in the third year (2015–2016), 370 individuals were recorded. In all re- smallest height class (0.1–0.2 m), suggesting that this could be a cruitment events, most of the individuals were concentrated in critical point for species survival. Manfredi (2014) found mortality the SE class between heights of 0.1–0.2 m (Fig. 5A). The fecundity rate for a P. lambertii population to be 23.66% and attributed it to rate was 4.007 (RP to SE) and 0.156 (RP to JV). The population soil compaction resistance owing to the presence of livestock. growth rate (␭) was 1.025, significantly higher than 1 (95% CI, Cattle grazing did occur in our study site, but mostly in open 1.016 < ␭ < 1.066). areas; therefore, other factors could be at play in this context. The correlations between canopy cover and the average num- Herbivory can be directly related to an individual’s mortality. ber of individuals present in the SE, JV, and IM classes were posi- During the four study years, SE individuals were found without tive and significant over the four study years (Fig. 6). leaves and apical buds, with clear signs of consumption by cater-

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Fig. 3. Distribution by height and diameter at breast height (dbh) classes of a Podocarpus lambertii population from Lages, Santa Catarina state, Brazil. Distribution of height classes for (A) seedling, (B) juvenile, (C) immature, and (D) reproductive classes. Distribution of dbh classes for (E) immature and (F) reproductive classes. For personal use only. Can. J. For. Res. Downloaded from www.nrcresearchpress.com by Mr. Alison Paulo Bernardi on 06/18/19

pillars. Caterpillars such as Epithecia spp. and Cyclophora annularis Pathogenic and saprophytic fungi such as the genera Pestalotia spp., (Felder & Rogenhofer, 1875) are known to feed on P. lambertii Penicillum spp., Phomopsis spp., Mucor spp., and Trichoderma spp. leaves, causing foliar losses up to 20% in adult individuals (Costa may cause nonviability and diseases in seeds and seedlings of and Boscardin 2014). Paludo et al. (2011) also suggested that her- P. lambertii (Garcia 2003). Finally, in lower frequency than her- bivory could play a role in the mortality of A. angustifolia seedlings bivory and presence of fungi, we found dead SE individuals under because of recent removal or absence of cotyledons and apical the dry leaves of A. angustifolia. Almost 60% of dry leaves found in buds. We found SE individuals to be completely defoliated and RP the MOF are from A. angustifolia, and leaf fall can kill seedlings of individuals presenting necrosis and dry branches, possibly from A. angustifolia and other species (Backes et al. 2005). It should be the presence of fungi. Neto (1979) reported that the fungus Corynelia noted that other factor such as excessive moisture and inter- and brasiliensis Fitzp. could infect seedlings and adults of P. lambertii, intra-specific competition may also cause mortality and should be causing necrosis, apical death, and premature loss of apical bud. studied.

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Fig. 4. Podocarpus lambertii population dynamics based on the average of three annual Lefkovitch matrices. Circles with continuous line represent the different classes (SE, seedling; JV, juvenile; IM, immature; RP, reproductive); circles with dotted lines represent permanence in the same class; horizontal continuous lines represent transition to next successive classes; and upper dashed lines represent fecundity of RP individuals.

Fig. 5. Distribution of seedling (SE) and juvenile (JV) height classes of a Podocarpus lambertii population from Lages, Santa Catarina, Brazil: (A) height class distribution for all recruits; (B) height class distribution for all dead individuals. Both classes were evaluated in a 2.56 ha plot between 2014 and 2016.

Fig. 6. Scatterplot and correlation between canopy cover and the average number of individuals in the Seedlings (SE), Juveniles (JV) and For personal use only. Immature (IM) classes. Black dots represents each subplot (10 × 10 m), and canopy cover was arcsine transformed. Can. J. For. Res. Downloaded from www.nrcresearchpress.com by Mr. Alison Paulo Bernardi on 06/18/19

Importance of forest patches to P. lambertii viduals of the species were found under forest patches, suggesting The conversion of grasslands to forests has global relevance, is that they provided adequate conditions (e.g., moisture, light, re- highly variable, and does not have a well-described pattern duced herbaceous competition, nutrients, microclimate) for the (Halpern et al. 2010). This theme has been studied from different species recruitment, germination, establishment, and growth. perspectives in which most of the studies have sought explana- A marked characteristic of southern Brazilian forest patches is tions for grasslands conversion to forests in extrinsic factors, e.g., the dominant presence of A. angustifolia, as found in our study site. overgrazing, livestock, fire presence, and climatic changes Araucaria angustifolia is a foundation species that ameliorates the (Scholes and Archer 1997; Haugo and Halpern 2007; Haugo and microenvironmental conditions facilitating the initial establish- Halpern 2010); however, biotic interactions can maintain and en- ment and growth of forests under its canopy (Duarte et al. 2006). hance grassland conversion and may play a role in population Podocarpus lambertii occurs in the understory layer, generally asso- dynamics of species (Halpern et al. 2010; Rice et al. 2012) such as ciated with A. angustifolia, and possibly benefits from these condi- the presence of forest patches. Our findings revealed that all indi- tions. In addition, P. lambertii is preferentially bird-dispersed

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(Kuniyoshi 1983) and may be favored by the perching effect that Acknowledgements forest patches provide (Duarte et al. 2006; Korndörfer et al. 2014). We thank José A.R. Ribeiro for allowing the study to be carried Several Podocarpus species are bird-dispersed (see Turner and out in his area. This work was supported by Coordenação de Aper- Cernusak (2011) and references therein), and the benefits of the feiçoamento de Pessoal de Nível Superior (CAPES) for Doctoral perching effect for species was already mentioned in a scholarships to A.P.B., M.B.L, and T.M., Conselho Nacional de seed rain study (Santos et al. 2011). Desenvolvimento Científico e Tecnológico (CNPq) for a Master Other abiotic conditions influenced by forest patches are soil scholarship to R.C.R. and Doctoral scholarships to M.P.H. and characteristics such as moisture, nutrients, and organic matter. M.S.R. (304724/2010-6), Fundação de Amparo à Pesquisa e Inovação Soil moisture can increase the probability of P. lambertii occur- do Estado de Santa Catarina (grant nos. 11939/2009, 18868/2011-9, rence (Longhi et al. 2010) and was a determinant in mortality, and TR2013-3558), and Programa de Apoio à Núcleos de Excelência recruitment, and survival of seedlings (Manfredi 2014). Moreover, (PRONEX, grant no. 2780/2012-4). We acknowledge the anony- soil moisture can accelerate and standardize the seed germina- mous reviewers and the Associate Editor for their valuable contri- tion process. Podocarpus lambertii has orthodox seeds, which butions to this manuscript. remain viable after dehydration (Garcia and Nogueira 2008); how- ever, orthodox seeds lose tolerance to desiccation in the early References stages, but when rehydrated, they maintain their physiological Adan, N., Atchison, J., Reis, M.S., and Peroni, N. 2016. Local knowledge, use and functions influencing the germination process (Guimarães et al. management of ethnovarieties of Araucaria angustifolia (Bert.) Ktze. in the Plateau of Santa Catarina, Brazil. Econ. Bot. 70(4): 353–364. doi:10.1007/s12231- 2011). In addition to altering soil moisture and structure, forest 016-9361-z. patches normally enhance soil nutrients (C, N, P, and cations; Archer, S., Scifres, C., Bassham, C.R., and Maggio, R. 1988. Autogenic succession Scholes and Archer 1997). Nurse plants such as A. angustifolia can in a subtropical savanna: conversion of grassland to thorn woodland. Ecolog- improve soil chemical conditions and may act as nutrient pumps, ical Monographs, 58(2): 111–127. Backes, A., Prates, F.L., and Viola, M.G. 2005. Produção de serapilheira em Flo- favoring the occurrence of seedlings under its canopy (Scholes resta Ombrófila Mista, em São Francisco de Paula, Rio Grande do Sul, Brasil. and Archer 1997; Korndörfer et al. 2014). Still related to soil char- Acta Bot. Bras. 19(1): 155–160. doi:10.1590/S0102-33062005000100015. acteristics, Manfredi (2014) observed higher recruitment and sur- Behling, H., Pillar, V.D., Orlóci, L., and Bauermann, S.G. 2004. Late Quaternary vival of P. lambertii individuals on steep slopes (≥7.8%), in deep soils Araucaria forest, grassland (Campos), fire and climate dynamics, studied by high-resolution pollen, charcoal and multivariate analysis of the Cambará do (>0.24 m), and in soils with less than 6.6% of organic matter. Sul core in southern Brazil. Palaeogeogr. Palaeoclimatol. Palaeoecol. 203(3–4): Light availability is another abiotic condition influenced by for- 277–297. doi:10.1016/S0031-0182(03)00687-4. est patches. Previous studies revealed that P. lambertii is shade- Behling, H., Jeske-Pieruschka, V., Schüler, L., and Pillar, V.D.P. 2009. Dinâmica dos tolerant, based on growth and frequency of individuals on dense campos no sul do Brasil durante o Quaternário Tardio. In Campos Sulinos — conservação e uso sustentável da biodiversidade. Edited by V. De Patta Pillar, understory (e.g., under forest patches), a lower ratio of chlo- S.C. Müller, Z.M. de Souza Castilhos, and A.V. Ávila Jacques. Ministério do Meio rophyll a to chlorophyll b, and greater leaf mass per area (Longhi Ambiente, Brasília, Brasil. et al. 2010; Fagundes 2010). Our results corroborate this aspect, at Boldrini, I.I. 2009. Biodiversidade dos campos do planalto das araucárias. In least in the initial life cycle stages, as all individuals of the species Campos Sulinos — conservação e uso sustentável da biodiversidade. Edited by V. De Patta Pillar, S.C. Müller, Z.M. de Souza Castilhos, and A.V. Ávila Jacques. occurred under the forest patches with a positive correlation be- Ministério do Meio Ambiente, Brasília, Brasil. pp. 63–77. tween canopy cover and average number of individuals in each Carvalho, P.D. 2004. Pinheiro-Bravo: Podocarpus lambertii. Embrapa Florestas- class (SE, JV, and IM). In addition, light availability through the Circular Técnica 95 (INFOTECA-E), Colombo, Paraná. pp. 1–9. Caswell, H. 2001. Matrix population models: construction, analysis, and inter- For personal use only. canopy of adults of A. angustifolia may improve the establishment pretation. 2nd ed, Sinauer Assoc., Inc., Publishers, Sunderland, Mass. of seedlings (limiting photoinhibition), without limiting the light Chalwell, S.T.S., and Ladd, P.G. 2005. Stem demography and post fire recruit- availability for seedling growth (Korndörfer et al. 2014). Thus, it is ment of Podocarpus drouynianus: a resprouting non-serotinous conifer. Bot. J. possible that seedlings and juveniles of P. lambertii have physiolog- Linn. Soc. 149(4): 433–449. doi:10.1111/j.1095-8339.2005.00454.x. ical and morphological adaptations that can allow better light CONSEMA. 2014. Official List of Threatened Species of Extinction in the State of Santa Catarina. State Council for the Environment of Santa Catarina. Avail- absorption and resource maintenance. Several species of Podocarpus able from http://www.sds.sc.gov.br/index.php/biblioteca/consema/legislacao/ have distinct behavior to light availability, which directly influ- resolucoes/325-resolucao-consema-no-512014-1/file [accessed 8 December ences the recruitment, establishment, and growth of species 2018]. Costa, E.C., and Boscardin, J. 2014. Occurrence of acicula-eating caterpillars on (Turner and Cernusak 2011). Thus, for P. lambertii, a better compre- Podocarpus lambertii Klotzsh ex Eichler in Southern Brazil. EntomoBrasilis, hension of light availability in different environments is neces- 7(3): 238–240. doi:10.12741/ebrasilis.v7i3.438. sary, as it is directly related to population dynamics of the species. Crone, E.E., Menges, E.S., Ellis, M.M., Bell, T., Bierzychudek, P., Ehrlén, J., Kaye, T.N., Knight, T.M., Lesica, P., Morris, W.F., Oostermeijer, G., Quintana-Ascencio, P.F., Conclusion Stanley, A., Ticktin, T., Valverde, T., and Williams, J.F. 2011. How do plant ecologists use matrix population models? Ecol. Lett. 14(1): 1–8. doi:10.1111/j.1461-0248. In the context of forest–grassland mosaics, the Podocarpus lambertii 2010.01540.x. population demonstrated growth over time, recruitment was Crone, E.E., Ellis, M.M., Morris, W.F., Stanley, A., Bell, T., Bierzychudek, P., and Oostermeijer, G. 2013. Ability of matrix models to explain the past and pre- high, mortality rate was low, and all individuals occurred under dict the future of plant populations. Conserv. Biol. 27(5): 968–978. doi:10.1111/

Can. J. For. Res. Downloaded from www.nrcresearchpress.com by Mr. Alison Paulo Bernardi on 06/18/19 forest patches. The species can be considered shade-tolerant, at cobi.12049. least in the initial life cycle stages, and characteristic of forest Dillingham, P.W., Moore, J.E., Fletcher, D., Cortés, E., Curtis, K.A., James, K.C., patches inside grasslands from the absence of individuals in open and Lewison, R.L. 2016. Improved estimation of intrinsic growth rmax for long-lived species: integrating matrix models and allometry. Ecol. Appl. areas. Forest patches are extremely important to P. lambertii for 26(1): 322–333. doi:10.1890/14-1990. promoting specific conditions, in particular, those related to Duarte, L.D.S., Dos-Santos, M.M., Hartz, S.M., and Pillar, V.D. 2006. Role of nurse light, that favor the population dynamics of the species. The eco- plants in Araucaria Forest expansion over grassland in south Brazil. Austral logical characteristics of this species and specific conditions pro- Ecol. 31(4): 520–528. doi:10.1111/j.1442-9993.2006.01602.x. vided by forest patches allow the population to continuously grow Enright, N.J., Miller, B.P., Perry, G.L., Goldblum, D., and Jaffré, T. 2013. Stress- tolerator leaf traits determine population dynamics in the endangered New in sufficient numbers to compensate for the observed mortality Caledonian conifer Araucaria muelleri. Austral Ecol. 39(1): 60–71. doi:10.1111/ rate. It is worth mentioning, however, that P. lambertii is a long- aec.12045. lived species, and the influences of the microenvironment, soils Fagundes, P.B. 2010. Estudo comparativo da tolerância ao sombreamento de characteristics, and abiotic interactions need to be studied, as Araucaria angustifolia e Podocarpus lambertii. Universidade Federal do Rio Grande do Sul, Brazil. they are vital for a better understanding of the population dynam- Farjon, A. 2013. Podocarpus lambertii. In The IUCN Red List of Threatened Species ics of this species. 2013: e.T34086A2844519. doi:10.2305/IUCN.UK.2013-1.RLTS.T34086A2844519.en.

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