Compared to tropical and temperate forests, the carbon balance of subtropical forests is not well studied. Trees in humid subtropical forests may maintain relatively high photosynthetic rates even during the cold periods owing to relatively mild seasonal low temperatures. This pattern was observed for some East Asian subtropical evergreen forests [1,2]. Leaf level results show that net CO2 assimilation in dominant evergreen species of an East Asian subtropical forest never dropped below 50% of their photosynthetic capacity [3,4]. At stand level, the forest sites had considerably high values of carbon sequestration, as respiratory losses declined strongly during the cold season . High year-round carbon sequestration suggests that these subtropical forests are among the largest carbon-sinks across terrestrial ecosystems. Subtropical forests are widespread in SE Asia, northern Australia and Argentina and are facing severe threats imposed by the expansion of tree plantations and agricultural lands.
The subtropical forests in northeastern (NE) Argentina are the southern portion of the Atlantic Forest Biome extending along the Atlantic coast of Brazil and southeastern Paraguay. Just a few centuries ago the Atlantic Forest was the second most extensive forest ecosystem in the Neotropics after the Amazonian forests. However, unlike the Amazonian forests, about 93% of the original cover of the Atlantic Forest has been lost due to human activities. Only small fragments of the subtropical Atlantic Forest remain in Brazil and Paraguay , while the largest stands of these forests are in Argentina. Despite the fact that most of this biome has been lost, the remnants still have high biological diversity and endemism and are included among the 25 top biodiversity hotspots in the world . During the last three decades, the area dedicated to tree plantations in Argentina has increased five-fold . Many humid subtropical forests in NE Argentina have been replaced recently by high-yield tree plantations of Eucalyptus and Pinus.
The temperature effects on the carbon balance of these forests have not been studied. Air temperatures of the subtropical Atlantic forests in Argentina drop considerably during the winter season but seldom reach freezing levels. The number of days with temperatures below 0 °C ranges from 0 to 12 per year . If these subtropical forests maintain high canopy photosynthesis throughout the year despite low temperatures during the cold season, they can have a high capacity for yearly carbon sequestration. Thus conservation and restoration of subtropical forests worldwide are of importance for the global carbon cycle.
In recent decades, information provided by remote sensing has emerged as a new and useful tool to study the spatial and temporal dynamics of vegetation [9,10,11,12]. Passive sensors provide information on the percentage of energy from the sun that is reflected by different land covers in different wavelengths of the electromagnetic spectrum. In the case of the vegetation, this information is usually summarized by spectral indices to assess traits related to the structure and function of terrestrial ecosystems. The normalized vegetation index (NDVI) is one of the most used spectral indices because it is closely related to the amount of photosynthetically active radiation intercepted by vegetation, and the amount of green biomass and chlorophyll content in leaves [13,14,15,16,17]. This spectral index may provide valuable information on the temporal dynamics of photosynthetic activity and primary productivity [12,18,19]. Remote sensing is also used to estimate canopy leaf area index (LAI, the total leaf area per unit ground area). This variable is a controlling biophysical property of vegetation functioning, and quantifying LAI is thus of importance for understanding energy, carbon and water ﬂuxes between the land surface and the atmosphere [20,21].
The main objective of this study was to assess the seasonal dynamics of NDVI and potential canopy photosynthetic activity in relation to seasonal changes in leaf area index (LAI), chlorophyll content, and air temperatures of NE Argentina subtropical forests, using remote sensing and field measurements. We also included, for comparative purposes, several plantations of Pinus, Eucalyptus and Araucaria that are known to have high yields and exhibit rather constant growth rates. Remote sensing was used to assess the seasonal dynamics of leaf pigments involved in carbon assimilation and total stand level gas exchange surface, and thus the spectral index used was considered to be a proxy of canopy photosynthetic activity. Stem growth rates, LAI and leaf chlorophyll concentration were monitored for the native forests and plantations. The subtropical forest studied is characterized by the coexistence of deciduous species with rapid growth rates and evergreen species with slower growth rates. The deciduous species are leafless during the mild winter season and thus the evergreen trees can use the relatively high incoming solar radiation when climatic conditions are more favorable for growth (temperatures closer to the optimum for CO2 assimilation). It was hypothesized that the NDVI values of humid subtropical forests in Argentina, as a measure of potential canopy photosynthetic activity, remains at high levels throughout the year, comparable to high-yield tree plantations.
2.1. Study Area
Native species from the Atlantic Forest within the Iguazú National Park of Misiones Province, NE Argentina (26°25′ S, 54°37′ W), and plantations of Pinus taeda, Pinus caribaea caribaea, a hybrid Pinus, Eucalyptus grandis and Araucaria angustifolia were monitored in this study. Mean annual rainfall in the area is 2000 mm and precipitation is evenly distributed throughout the year. Although there is not a dry season, some climatic anomalies can occur in some years such as a decrease in precipitation during few consecutive weeks triggering short-term drought effects. Mean annual temperature is 21 °C, with monthly means of 25 °C in January and 15 °C in July, representing the warmest and coldest months of the year, respectively. The soils are derived from basaltic rocks, containing high concentration of Fe, Al and Si and correspond to the 9a type according to local descriptions , which are mostly ultisols .
2.2. Field Measurements
Leaf Area Index (LAI), leaf chlorophyll concentration and stem growth were monitored in stands of the native forests and four tree plantations (Eucalyptus grandis, Araucaria angustifolia, Pinus taeda and Pinus caribaea caribaea). Measurements were done in March and July 2013, corresponding to late summer–early autumn and winter seasons, respectively.
Leaf area index (LAI) was calculated by a nondestructive method by measuring incoming light below the canopy and in an open area with the AccuPAR Lp-80 ceptometer (Decagon Devices, Pullman, WA, USA) at ten points randomly selected in each tree plantation and thirty points in the native forest stand. The Chlorophyll Meter SPAD 502 meter (Minolta, Japan) was used to estimate leaf chlorophyll concentration [24,25]. Three individuals were used in each of the tree plantations while in the native forests one tree of five different species was used: Balfourodendron riedelianum, Cedrela fissilis, Ceiba speciosa, Cordia trichotoma and Chrysophyllum gonocarpum (Table 1). Values of SPAD units obtained from 30 leaves of each species were converted to chlorophyll concentration in µg cm−2 using the equation of Pinkard et al.  for E. grandis and Coste et al.  for the remaining species. Chlorophyll concentration and LAI measurements were done at the same time.
Ten species were selected and ten individuals per species were used to measure stem radial growth in the native forests and in the tree plantations. Dendrometer bands were installed on all selected trees. Dendrometers were made manually and consisted of a stainless steel tape encircling a tree stem, with one end passing through a collar (which is attached to the other end) and connected back to itself with a stainless steel spring, as described by Cattelino et al. . Three months after dendrometer installation (allowing for stem-dendrometer adjustment) a permanent mark was made on the metal band next to the collar. As stem circumference increases, the mark moves away from the collar and the spring is stretched, keeping the dendrometer tight. A flexible ruler was used to measure stem circumference changes with an accuracy of 0.5 mm. Stem circumference was recorded monthly from February 2012 to March 2013. Stem diameter increments were used as a proxy of stem growth and it was expressed as change in stem diameter with respect to the initial value at the beginning of the measurements.
Table 1. List of tree species studied, their family, native or exotic origin, and leaf phenology.
|Rutaceae||Balfourodendron riedelianum (Engl.) Engl.||Native||Brevideciduous|
|Meliaceae||Cabralea canjerana (Vell.) Mart.||Native||Evergreen|
|Meliaceae||Cedrela fissilis Vell.||Native||Deciduous|
|Bombacaceae||Ceiba speciosa (A.St.-Hil., A.Juss. & Cambess.) Ravenna||Native||Deciduous|
|Boraginaceae||Cordia trichotoma (Vell.) Arráb. ex Steud.||Native||Deciduous|
|Fabaceae||Holocalyx balansae Micheli||Native||Evergreen|
|Lauraceae||Ocotea diospyrifolia (Meisn.) Mez.||Native||Evergreen|
|Fabaceae||Lonchocarpus muehlbergianus Hassl.||Native||Brevideciduous|
|Fabaceae||Parapiptadenia rígida (Benth.)Brenan||Native||Brevideciduous|
|Sapotaceae||Chrysophyllum gonocarpum (Mart. & Eichler) Engl.||Native||Evergreen|
|Araucariaceae||Araucaria angustifolia (Bertol.) Kuntze||Native||Evergreen|
|Myrtaceae||Eucalyptus grandis W.Hill ex Maiden||Exotic||Evergreen|
|Pinaceae||Pinus elliotti elliotti × P. caribaea hondurensis (hybrid Pinus)||Exotic||Evergreen|
|Pinaceae||Pinus taeda L.||Exotic||Evergreen|
2.3. Remote Sensing and Meteorological Variables
The Terra MODIS sensor (Moderate Resolution Imaging Spectroradiometer) is a 36-band spectroradiometer that measures visible and infrared radiation from 0.4 to 14.5 µm. The individual spectral bands have different spatial and temporal resolutions. The measurements made by the MODIS sensor yield data used to develop different products, e.g. vegetation indices, productivity estimates, land surface cover, fire occurrence [27
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