Phenology and Tree Radial Growth of Schinus terebinthifolius in a Subtropical Forest

Jaçanan Eloisa de Freitas Milani Rodrigo de Andrade Kersten Tomaz Longhi - Santos Franklin Galvão Erika Amano Carlos Velozzo Roderjan Maria Raquel Kanieski About the authors

Abstract

During a period of 5 years, we monthly monitor the phenology and the stem diameter increment of 12 of Schinus terebinthifolius trees. Dendrometer bands were used for it. This study was aimed to answer the following questions: (i) Are there conflicting demands for resource allocation in different phenophases? (ii) In which period does the stem diameter increment occur? (iii) Which phenophases are more likely related to stem radial growth? The phenological observations were carried out using the Activity Index. In order to identify patterns in phenology and diameter increment over the assessment period (2010-2015), we performed an analysis of seasonal decomposition, followed by Pearson’s correlation analysis. Apparently, there is no conflicting demand for resources, but an optimized distribution of them, regulated mainly by the allocation of nutrients derived from leaf senescence, as well as, temperature rise and photoperiod. Higher diameter growth rates occurred from December to March which coincided with the flowering period.

Keywords:
Demand; Flowering; Increment; Plasticity; Resources

1. INTRODUCTION

The relationship between plant phenology and growth in both tropical and subtropical forests in South America has been very little explored (O’brien et al., 2008O’brien JJ, Oberbauer SF, Clark DB, Clark DA. Phenology And Stem Diameter Increment Seasonality In A Costa Rican Wet Tropical Forest. Biotropica 2008; v. 40, n. 2, p. 151-159. ), and also scientific knowledge of alluvial environments is even more scarce. In addition, understanding the dynamics of alluvial environments in different biomes remains a major challenge in ecology. In the Brazilian Atlantic Forest, the remaining fragments are mostly small, isolated and composed of disturbed secondary vegetation, comprising less than 50 ha (Ribeiro et al.,2009Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM. The Brazilian Atlantic Forest: How Much Is Left, And How Is The Remaining Forest Distributed? Implications For Conservation. Biological Conservation 2009; 142, n. 6, p. 1141-1153.). The landscape connectivity favors biological processes for the survival of populations and interactions among species (Metzger et al., 2009Metzger JP, Martensen AC, Dixo M, Bernacci LC, Ribeiro MC, Teixeira AMG, Pardini R. Time-Lag In Biological Responses To Landscape Changes In A Highly Dynamic Atlantic Forest Region. Biological Conservation 2009; v. 142, n. 6, p. 1166-1177.). Actually, forest corridors are considered the best-known factors to reduce the negative effects of fragmentation (Lees and Peres, 2008Lees A C, Peres CA. Conservation Value Of Remnant Riparian Forest Corridors Of Varying Quality For Amazonian Birds And Mammals. Conservation Biology 2008; v. 22, n. 2, p. 439-449.). In this context, riparian vegetation, currently protected under laws and regulations by means of “Areas of Permanent Protection”, (APPs) plays a very important role in the preservation of such ecosystems. Therefore, further studies on the ecological aspects of riparian vegetation are required for the establishment of environmental conservation strategies as they will benefit future generations.

Tree growth is controlled by endogenous factors such as the plant genotype (Anderson et al., 2012Anderson JT, inouye DW, Mckinne AM, Colautti RI, Mitchell-Olds T. Phenotypic Plasticity And Adaptive Evolution Contribute To Advancing Flowering Phenology In Response To Climate Change. Proceedings Of The Royal Society Of London B 2012; Biological Sciences, 2 v. 279, n. 1743, p. 3843-3852.) and physiological processes (Pallardy, 2006Pallardy S. G. Physiology Of Woody Plants. Academic Press. 2006), as well as exogenous factors which are regulated by the availability of water and light (Gričar, 2013Gričar J. Influence Of Temperature On Cambial Activity And Cell Differentiation In Quercus Sessiliflora And Acer Pseudoplatanus Of Different Ages. Drvna Industrija 2013; v. 64, n. 2, p. 95-105.). Growth can usually be measured by repetitive measurements of the tree dimensions, which is most commonly performed by monitoring the stem diameter increment (Turner, 2001Turner IM. The Ecology Of Trees In The Tropical Rain Forest. Cambridge University Press. 2001.). These factors play a fundamental role on the growth of trees, which are linked to plant phenology and are evaluated by their phenological behavior (Morellato et al., 2000Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC Zipparro VB. Phenology Of Atlantic Rain Forest Trees: A Comparative Study. Biotropica 2000; v. 32, n. 4b, p. 811-823. ).

In tropical forests, climate temperature, light, and rainfall are the factors that most regulate fluctuations in primary and secondary growth of the plants and may be related to small environmental changes, such as rainfall variations and day length. (O’brien et al., 2008O’brien JJ, Oberbauer SF, Clark DB, Clark DA. Phenology And Stem Diameter Increment Seasonality In A Costa Rican Wet Tropical Forest. Biotropica 2008; v. 40, n. 2, p. 151-159. Borchert et al., 2005Borcher TR, Renner SS, Calle Z, Navarrete D. Photoperiodic Induction Of Synchronous Flowering Near The Equator. Nature 2005; v. 433, n. 7026, p. 627., Marques and Oliveira, 2004Marques MC, OLIVEIRA PEAM. Fenologia De Espécies Do Dossel E Do Sub-Bosque De Duas Florestas De Restinga Na Ilha Do Mel, Sul Do Brasil. Revista Brasileira De Botânica 2004; v. 27, n. 4, p. 713-723. Wright and Van Schaik, 1994Wright SJ, Van Schaik CP.; Light And The Phenology Of Tropical Trees. American Naturalist 1994; v. 143, n. 1, p. 192-199.). In temperate forests, climatic conditions, especially low temperatures, are the main factors that control the dynamics of tree growth (Morel et al., 2015Morel H, Mangenet T, Beauchêne J. Ruelle J, Nicolini E, Heuret P, Thibaut B. Seasonal Variations In Phenological Traits: Leaf Shedding And Cambial Activity In Parkia Nitida Miq. And Parkia Velutina Benoist (Fabaceae) In Tropical Rainforest. Trees 2015; v. 29, n. 4, p. 973-984.).

The relationship between phenology and growth of some tropical forest species has been evaluated and reported by Worbes (1995)Worbes M. How to measure growth dynamics in tropical trees a review. Iawa Journal 1995; v. 16, n. 4, p. 337-351. O’Brien et al. (2008)O’brien JJ, Oberbauer SF, Clark DB, Clark DA. Phenology And Stem Diameter Increment Seasonality In A Costa Rican Wet Tropical Forest. Biotropica 2008; v. 40, n. 2, p. 151-159. Yáñez-Espinosa et al. (2010)Yáñez-Espinosa L, Terrazas T, López-Mata L. Phenology and radial stem growth periodicity in evergreen subtropical rainforest trees. Iawa Journal 2010.v. 31, n. 3, p. 293-307., among others. However, no study has been found relating between phenology and growth in alluvial or hydromorphic soil environments, which main characteristic is temporarily water-saturated soil, caused by shallow water tables.

Plant resource allocation is typically associated with growth and reproduction, which might represent conflicting demands by plants (Barbour et al., 1999Barbour MG, Burk JH, Pitts WD, Gillian FS, Schwartz, MW. Allocation And Life History Patterns. Terrestrial Plant Ecology 1999; Third Edition. Benjamin Cummings. An Imprint Of Adison Wesley Longman, Inc. Pp, 88-116.). Furthermore, resource allocation in plants appears to be related to three key processes: (1) resources are simultaneously allocated to produce energy, growth and self-maintenance throughout the growing season, (2) most of the resources are allocated up to the beginning of the growing season and only later that such resources are allocated to reproduction, (3) the reproduction is shifted to the period of higher nutrient availability for the plants (Bazzaz et al., 2000).

According to these issues, this study was developed based on the premise that a given effort in plants is divided between growth and reproduction in a competing manner, in which resource allocation has to achieve optimal trade-offs on each of the processes. More specifically, the present study seeks to answer the following questions: (i) Are there conflicting demands for resource allocation in different phenophases? (ii) Do reproductive phenophases cause decrease in the stem diameter increment? (iii) In which period does the diameter increment occur? (iv) Which phenophases are more likely related to stem radial growth?

2. MATERIALS AND METHODS

2.1. Characterization of the study area

The study was performed in a fragment of Alluvial Araucaria Forest, within the Brazilian Atlantic Forest geographical coordinates 25º34’02,5” S and 49º20’53,5” W, in the Municipality of Araucaria, in the State of Parana, Brazil (Figure 1).

Figure 1
Location of the study area.

According to the classification of Köppen, the study area climate is humid subtropical mesothermal (Cfb), with a mean annual rainfall between 1,300-1,500 mm, without dry season and frequent frost occurrences in the winter. From January 2010 to December 2015, the monthly average temperature ranged from 12.2 °C in July (the coldest month) to 28.2 °C in February (the hottest month) (Figure 2). During the study period the average temperature was 17.7 °C.

Figure 2
Climate chart, data provided by SIMEPAR Weather Station. Average monthly temperatures (minimum, average, maximum) (lines) and monthly rainfall values (blue bars) between 2010-2015.

The soil in the study area is composed of fine-grained sediments, classified as Gleysol (Barddal et al., 2005) and poorly drained under natural conditions according to Brazilian soil classification system (Embrapa, 2013).

Schinus terebinthifolius (Anacardiaceae), also known as aroeira or pink pepper, it’s another important tree species in the remnant as it’s a pioneer in wide dispersion, found in almost all Brazilian States and ecosystems, from the Restingas of Rio Grande do Sul State up to the dry forests of Rio Grande do Norte State (Flora of Brazil, 2016). S. terebinthifolius is commonly found in river banks, streams and wet meadows. However and interestingly, it also occurs in dry land with low nutrient availability. Unlike Araucaria Araucaria angustifolia (Bert.) O. Kuntze, a notable species within mixed rainforests of Brazil, it is intolerant to hydromorphic soil, but it does not occur in such areas.

S. terebinthifolius shows great phenotypic plasticity based on its ability to successfully grow in diverse habitats in different places, not only in South America but also in Central and North America. Moreover, in the United States, this species has been introduced as an ornamental plant but it has become a major threat to ecosystems and it was then listed among invasive species (Williams et al., 2007Williams DA, Muchugu E, Overholt WA, Cuda JP. Colonization Patterns Of The Invasive Brazilian Peppertree, Schinus Terebinthifolius, In Florida. Heredity 2007;v. 98, n. 5, p. 284.).

2.2. Phenological behavior

It was randomly selected 12 individuals of S. terebinthifolius, which had their phenological behavior monthly monitored using binocular. The phenological vegetative and reproductive stages were registrated based on the Activity Index (Newstrom et al., 1994Newstrom LE, frankie GW, Baker HG. A New Classification For Plant Phenology Based On Flowering Patterns In Lowland Tropical Rain Forest Trees At La Selva, Costa Rica. Biotropica 1994; p. 141-159.), which considerates the presence-absence of a particular phenophase, on a scale of 0 (absence) to 1 (presence).

2.3. Stem diameter increment

All specimens were mounted with dendrometer bands (Mariaux, 1977Mariaux, A. Marques Et Rubans Dendroètres. Information Technique, 238. 1977. Worbes, 1995Worbes M. How to measure growth dynamics in tropical trees a review. Iawa Journal 1995; v. 16, n. 4, p. 337-351.) made of stainless steel with an accuracy of ± 0.20 mm, which were fixed at breast height (1.30 m) for continuous measurements of tree radial increment. Data were subsequently converted into tree stem diameters.

The monitoring of diameter increments and phenophase cycles were carried out concurrently for a 60-month period, between June 2010 and July 2015.

2.4. Data analysis

In order to identify the phenology behavior and the diametric increment throughout the assessment period, it was used the seasonal decomposition, considering the behavior of the month pattern for the variables (12-month period), into the additive model used (Collado et .al, 2017Collado DP, Valdés JAB, Molento MB, Gil ÁV, Pérez NI, Cruz AA, Campbell AA. Seasonal Behavior of Fasciola hepatica in Sacrificed Bovines at Chacuba Slaughterhouse, Camagüey, Cuba. Revista de Producción Animal, (2017); 29(1), 31-36.). The method divides time series into three components: trend-cycle, seasonality, and irregularity (Cleveland et al., 1990Cleveland RB, Cleveland WS. Terpenning I. A Seasonal-Trend Decomposition Procedure Based On Loess. Journal Of Official Statistics 1990; v. 6, n. 1, p. 3-73.). Our approach was focused only on the seasonality. The variables analyzed were: tree budding, leaf senescence, mature leaf, flowering, fruiting and diameter increment. By applying this technique, the annual average is transformed into zero and the seasonal indices (positive or negative) show the balance throughout the year. Negative numbers do not necessarily indicate the absence or loss but values below average.

Based on such indices, generated by analyzing seasonal decomposition, we used test Pearson’s correlation analysis to identify the relationship between the phenological variables and the increment. Data were tested at 95% confidence level. All statistical analyses were made with Statgraphics.

3. RESULTS

3.1. Phenology

Schinus terebinthifolius showed a pattern of continuous leaf production, more intensively from September to April. It was observed an annual cycle of phenophases, but not necessarily with the same intensity. Generally, there was little variation relating to leaf production, maintenance, and replacement among the study years (Figure 3).

Figure 3
Vegetative and reproductive phenological behavior of Schinus terebinthifolius in hydromorphic soil environment for a 5-year period.

The Flowering occurred from October to February, with a peak of blooming in December and January. The flowering period coincided over the 5-year survey, except for intensity variation among years. Fruiting was observed from January to March, simultaneously with the flowering period. However, March showed the highest fruiting incidence.

3.2. Diameter increment

The average monthly increment of tree diameter was 0.54 mm within the 60- month assessment, and the species cumulative diameter growth occurred from November to February (Figure 4). Overall, the monthly increment ranged from -1.08 to 2.25 mm. However, our findings showed that stem radial growth rates were significantly lower in August. The resumption of growth coincided with photoperiod increase.

Figure 4
Relationship between photoperiod and the average diameter increment of Schinus terebinthifolius in hydromorphic soil environment within a 5-year period.

The resumption of growth occured after August, maily between November and February. Nevertheless, it does not mean that throughout the other months the species trees ceased to grow in diameter, but the growth rates were lower (Figure 5).

Figure 5
Cumulative diameter growth of 12 specimens of Schinus terebintifolius in hydromorphic soil environment for a 5-year period.

Apparently, S. terebinthifolius showed concurrent periods of flowering and higher diameter growth rates. As to the fruiting, it began in the half of the highest increment period (Figure 6).

Figure 6
Growth and reproductive phenology of Schinus terebinthifolius in hydromorphic soil environment.

3.3. Seasonal decomposition

The estimated seasonal indices shown in Table 1 represent the effect of each season over the species radial growth as well as the respective magnitudes of events. Our results showed that the phenophases assessed during the time series were seasonal related and occurred in the same period of each year. In general, the phenology index values were lower on the second semester, and phenological activities were significantly more intense between January and April of each year.

Table 1
Seasonal indices of vegetative and reproductive phenophases as well as diameter increment of Schinus terebinthifolius. The four major values are shown in bold and the four lower ones are underlined.

Tree budding began in November, month in which we also recorded high rates of senescent leaves. Therefore, the rates of mature leaves only increased from December onwards. Although the budding peaks occur almost alternately in the subsequent months, the mature leaf rates remained high, likely due to no leaf fall in such period. Reproductive phenophases occurred from December to April of each year, but the flowering was more intense between December and March. Also, it was observed that the diameter increment coincided with the flowering period.

Resource allocation for stem radial growth was higher in January and lower in July. Furthermore, based on the data of seasonal decomposition shown in Table 1, we observed an even distribution of resources for both diameter increment and flowering.

In fact, the correlation test Pearson proved the direct relationship between diameter increment and flowering (p = 0.81 < 0.005). Such strong correlation indicates that the flowering season also marks the beginning of the diameter increment period.

4. DISCUSSION

4.1. Phenology

Plant development and survival have been often quantified and compared with conventional measurements based on individual characteristics (Mckown et al., 2013Mckown AD, Guy RD, Azam MS, Drewes EC, Quamme L K. Seasonality And Phenology Alter Functional Leaf Traits. Oecologia 2013; v. 172, n. 3, p. 653-665.). As seasonal or cycle events occur in plants, several ecophysiological relationships are established (Ackerly, 2004Ackerly DD. Adaptation, niche conservatism, and convergence: comparative studies of leaf evolution in the California chaparral. The American Naturalist 2004;v. 163, n. 5, p. 654-671. Pau et al., 2011Pau S, Wolkovich EM, Cook BI, Davies TJ, Kraft NJ, Bolmgren K. Predicting Phenology By Integrating Ecology, Evolution And Climate Science. Global Change Biology 2011; v. 17, n. 12, p. 3633-3643. ) and might be studied, because they interfere with the plant resource reorganization for both growth and development efforts.

Our findings showed phenological patterns relating to vegetative and reproductive phenophases, which occurred in overlapping periods. Schinus terebinthifolius presents a pattern of intermittent budding and frequent periods of leaf senescence. This species is not deciduous and has leaves during the whole year, in spite of a higher leaf fall between September and November.

Thus, in environments with low climate seasonality and without defined dry season, leaf fall and continuous budding would be the most advantageous strategies for such plant species, by allowing senescent leaves to remain attached to branches until the uptake and transport of nutrients (Jackson, 1978Jackson, J. F. Seasonality Of Flowering And Leaf-Fall In A Brazilian Subtropical Lower Montane Moist Forest. Biotropica 1978; v. 10, n. 1, p. 38-42. ). It would also contribute to the maintenance of photosynthetic rates along the whole year (Wagner et al., 2016Wagner FH. et al. Climate Seasonality Limits Leaf Carbon Assimilation And Wood Productivity In Tropical Forests. Biogeosciences 2016; v. 13, n. 8, p. 2537-2562.).

As reported in this study, the process of leaf senescence and later leaf fall occurring over the high rainfall months of October, November, December, January and February is crucial to satisfy plant nutrition needs, either by the nutrient redistribution prior to leaf fall or the nutrition intake derived from decomposition of soil organic matter (Bazzaz and Ackerly, 1992Bazzaz FA, Ackerly DD. Reproductive Allocation And Reproductive Effort In Plants. Seeds: The Ecology Of Regeneration In Plant Communities 1992; v1, 26.). Plant nutrition demand may be achieved by photosynthesis and nutrient intake, as well as the recycling of products degraded by senescent leaves (Gregersen et al,. 2008Gregersen PL, Holm PB. Krupinska K. Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biology, 2008 10, 37-49.). Reallocating resources from leaf fall seems to play a major role, so that phenophases and radial growth can be more efficient relating to this species.

Flowering periodicity over tropical regions varies a lot. However, if a species has a longer flowering period which coincides with leaf renewal cycle, it might also be beneficial to the reproductive success of the species, by adjusting to extreme climate conditions (drought or precipitation excess), lack of pollinators or a strategy of protection against herbivore attack (Pallardy, 2006Pallardy S. G. Physiology Of Woody Plants. Academic Press. 2006).

The high correlation between flowering and stem diameter increment in this study corroborates that the reproductive phenophase may trigger tree radial growth. This behavior has also been reported to other tropical species, to which phenological events may occur simultaneously (Lieth, 1974Lieth H. Purposes Of A Phenology Book. In Phenology And Seasonality Modeling. Springer Berlin Heidelberg 1974; (Pp. 3-19). ) as far as radial growth is concerned. In a study performed in the Amazon rainforest, Schöngart et al. (2002Schöngart J, Piedade MTF, Ludwigshausen S, Horna V, worbes M. Phenology And Stem-Growth Periodicity Of Tree Species In Amazonian Floodplain Forests. Journal Of Tropical Ecology 2002; v.18, n.4, p. 581-597.) has reported that the radial growth coincides with the beginning of budburst. According to Bordiert (1994), stem diameter increment in tropical forests is associated with budding and the beginning of flowering. It also corroborates Yáñez-Espinosa et al. (2010Yáñez-Espinosa L, Terrazas T, López-Mata L. Phenology and radial stem growth periodicity in evergreen subtropical rainforest trees. Iawa Journal 2010.v. 31, n. 3, p. 293-307.), to whom budburst and flowering are directly linked to radial growth while assessing phenology and growth periodicity of perennial trees within subtropical forests.

4.2. Stem diameter increment

The average growth rate of 4.94 mm/year observed in S. terebinthifolius is typical for tropical forest species, to which annual radial growth ranges from 0.5 to 6 mm, reaching up to 15 mm (Turner, 2001Turner IM. The Ecology Of Trees In The Tropical Rain Forest. Cambridge University Press. 2001.). Our findings showed that the radial growth varied over the course of five years. Such variations might be due to environmental seasonalities of temperature or soil water availability. It is worth mentioning that the study area is in a flood plain covered by an alluvial forest, where shortage of available water is not a limiting factor, unless severe climate events (drought or floods) occur. Consequently, rainfall did not show to be a key factor for diameter growth, although it might play an important role since S. terebinthifolius had the highest diameter increment rates under conditions of higher water availability (Figure 3) associated with photoperiod and higher temperatures.

Moreover, studies focused on tree rings as indicators of growth of subtropical species have indicated that lower temperatures are limiting factors for radial growth (Oliveira et al., 2010Oliveira JM, Roig FA, Pillar VD. Climatic Signals In Tree - Rings Of Araucaria Angustifolia In The Southern Brazilian Highlands. Austral Ecology 2010; v. 35, n. 2, p. 134-147. Longhi-Santos, 2013Longhi-Santos, T. Dendroecologia De Sebastiania Commersoniana (Baill.), L.B.Sm. And Downs Em Um Fragmento De Floresta Ombrófila Mista Aluvial, Paraná, Brasil. 2013. Dissertação Universidade Federal do Paraná.). During autumn and winter seasons, low temperatures induce a direct metabolic depression (dormancy), while increase in temperature induces significant tree-ring growth.

It is important to point out that over a 5-year period, there were significantly lower increment rates in August of each year, resulting in bark reduction due to lower moisture content (Kanieski et al., 2013Kanieski MR, Longhi-Santos T, MilanI J E F, Miranda B P, Galvão F, Botosso PC, Roderjan CV. Crescimento Diamétrico De Blepharocalyx Salicifolius Em Remanescente De Floresta Ombrófila Mista Aluvial, Paraná. Floresta e Ambiente 2013;. v. 20, n. 2, p. 197-206.). August is the driest month of the year in the study area, with lower rainfall (Figure 1). Such bark reduction was verified on the dendrometer bands prior to the season of higher growth as well as temperature and rainfall rise.

Plant dynamics, in terms of resource allocation demands, might be conflicting to favor a phenological activity over another (Begon et al., 2006Begon M, Townsend CRH, John L, Colin RT, John LH. Ecology: From Individuals To Ecosystems 2006; (No. Sirsi) Isbn-13: 978-1-4051-1117-1.) and, in turn, it may endanger such activities. However, based on the data of seasonal decomposition, this phenomenon was not observed in the present study. On the other hand, we observed that both reproduction and growth occurred at the same time range during a 5-year period (Table 1).

According to our findings, it seems that the flowering event triggers the resumption of higher radial growth of S. terebinthifolius. The stem diameter increment of this species is also associated with temperature rise, photoperiod and volume of rainfall.

5. CONCLUSION

Considering Schinus terebinthifolius:

Apparently, there was no conflicting demand for resources, but an optimized distribution of them, regulated mainly by the allocation of nutrients derived from leaf senescence, temperature, and photoperiod (question I).

Reproductive phenophases did not cause a reduction in the diametric increment (question II).

The monthly increment of the specie diameter growth occurred from November to February (question III).

Schinus terebinthifolius allocated its resources for growth and reproduction simultaneously when growing on a hydromorphic soil. Diameter increment was intrinsically related to the flowering phenophase (question IV).

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Publication Dates

  • Publication in this collection
    02 Sept 2020
  • Date of issue
    2021

History

  • Received
    06 May 2020
  • Accepted
    05 Aug 2020
Instituto de Florestas da Universidade Federal Rural do Rio de Janeiro Rodovia BR 465 Km 7, CEP 23897-000, Tel.: (21) 2682 0558 | (21) 3787-4033 - Seropédica - RJ - Brazil
E-mail: floram@ufrrj.br