remote sensing

Article
Mapping Periodic Patterns of Global Vegetation
Based on Spectral Analysis of NDVI Time Series
Laura Recuero 1,2 , Javier Litago 3 , Jorge E. Pinzón 4 , Margarita Huesca 5 , Maria C. Moyano 6 and
Alicia Palacios-Orueta 1,2, *
1 Departamento de Sistemas y Recursos Naturales, ETSIMFMN, Universidad Politécnica de Madrid,
C/José Antonio Novais 10, 28040 Madrid, Spain; laura.recuero@upm.es
2 Centro de Estudios e Investigación para la Gestión de Riesgos Agrarios y Medioambientales (CEIGRAM),
Universidad Politécnica de Madrid, C/Senda del Rey 13, 28040 Madrid, Spain
3 Departamento de Economía Agraria, Estadística y Gestión de Empresas, ETSIAAB, Universidad Politécnica
de Madrid, Avenida Complutense 3, 28040 Madrid, Spain; javier.litago@upm.es
4 Science Systems and Applications Inc., Biospheric Sciences Laboratory, NASA Goddard Space Flight Center,
Code 618, Greenbelt, MD 20771, USA; jorge.e.pinzon@nasa.gov
5 Land, Air and Water Resources Department, Center for Spatial Technologies And Remote Sensing (CSTARS),
University of California Davis, One Shields Avenue, Davis, CA 95616, USA; mhuescamartinez@ucdavis.edu
6 Departamento de Ingeniería Agroforestal, ETSIAAB, Universidad Politécnica de Madrid, Avenida
Complutense 3, 28040 Madrid, Spain; mariacarmen.moyano@upm.es
* Correspondence: alicia.palacios@upm.es; Tel.: +34-910671745




Received: 24 September 2019; Accepted: 18 October 2019; Published: 25 October 2019


Abstract: Vegetation seasonality assessment through remote sensing data is crucial to understand
ecosystem responses to climatic variations and human activities at large-scales. Whereas the study of
the timing of phenological events showed significant advances, their recurrence patterns at different
periodicities has not been widely study, especially at global scale. In this work, we describe vegetation
oscillations by a novel quantitative approach based on the spectral analysis of Normalized Difference
Vegetation Index (NDVI) time series. A new set of global periodicity indicators permitted to identify
different seasonal patterns regarding the intra-annual cycles (the number, amplitude, and stability) and
to evaluate the existence of pluri-annual cycles, even in those regions with noisy or low NDVI. Most
of vegetated land surface (93.18%) showed one intra-annual cycle whereas double and triple cycles
were found in 5.58% of the land surface, mainly in tropical and arid regions along with agricultural
areas. In only 1.24% of the pixels, the seasonality was not statistically significant. The highest values
of amplitude and stability were found at high latitudes in the northern hemisphere whereas lowest
values corresponded to tropical and arid regions, with the latter showing more pluri-annual cycles.
The indicator maps compiled in this work provide highly relevant and practical information to
advance in assessing global vegetation dynamics in the context of global change.

Keywords: land surface phenology; vegetation dynamics; spectral analysis; periodogram; NDVI;
seasonality; stability; pluri-annual cycles; bioclimate

1. Introduction
Seasonal environmental transitions are one of the most predictable variability that ecosystems
experience. For example, temperate plants tend to adjust seasonally in response to the changing length
of day (photoperiod), exhibiting a relatively predictable phenological timing of production and loss
of leaves, flowers and fruits [1]. The recurrence of phenological cycles results in periodic vegetation
patterns becoming a distinctive trait of ecosystems [2,3] with different levels of regularity at intra- and
inter-annual time scales. To understand vegetation periodicities, in the present research we adopt the

Remote Sens. 2019, 11, 2497; doi:10.3390/rs11212497 www.mdpi.com/journal/remotesensing

Remote Sens. 2019, 11, 2497 2 of 21

definition of seasonality introduced by Hylleberg [4] (p.4) ‘Seasonality is the systematic, although not
necessarily regular, intra-year movement caused by the changes of the weather, . . . ’, and we adapt it to
an ecological context by adding other factors with influence in vegetation dynamics such as phenology,
physical conditions or anthropogenic activities. In addition, when long-term data is available it is
common to observe lower frequency periodic patterns whose length exceeds one or several years,
commonly known as pluri-annual cycles [5] which are highly dependent on weather, particularly on
rainfall–drought cycles. These two factors have been found significantly related to the 11-year solar
cycle at some individual meteorological stations [6] and nowadays it is well known that these events
are often spatially link across very distant regions through different teleconnections patterns [7].
Vegetation seasonality has a significant effect on land surface functioning. At local scales, the
behavior of many birds and insects species are synchronized with vegetation seasonal variations [8,9]
with significant disequilibrium when seasonality is altered [10–12]; at larger scales, vegetation
seasonality plays a key role in biogeochemical cycling and energy fluxes with a strong impact on
atmospheric composition and variability [13–16]. Accurate parameterization of vegetation dynamics
by developing indicators of periodic patterns (e.g., related to the amplitude and stability of cycles)
can help to improve models making it possible to strengthen our understanding of vegetation-climate
interactions [17–19]. This is critically important in the current scenario of global change that may alter
ecosystem dynamics by changing expected climate conditions and increasing the frequency of climatic
extreme events (floods, heat waves, droughts) [20,21]. The extent and ubiquitous impact of global
change processes makes necessary the development of tools to understand and operatively quantify
the periodicity of phenological patterns and its relationship to climatic and other environmental drivers
at large scales.
Several factors can affect the periodic patterns of vegetation. Firstly, climate limits plant growth
with different precipitation, temperature and radiation regimes [22–24] strongly influencing vegetation
seasonality and inter-annual cycles. Secondly, human activities and natural disturbances such as
agricultural irrigation, land use changes, pests or fires, can alter seasonal vegetation patterns [25]
with slight effects such as changes in seasonality stability or stronger effects such as the number of
intra-annual cycles or the appearance of abrupt changes.
Spectral analysis as a part of time series analysis [26] is probably the most extensively used
methodology to detect, identify, assess and model periodicities in time series. It has been widely applied
in disciplines such as meteorology [27], astronomy [28], economy and agriculture [5], engineering
or mathematics [29–31]. The Fourier spectral analysis [32] decomposes time series into sinusoidal
functions at different frequencies providing a quantitative assessment of the relevance (i.e., power) of
each periodic component which is known as spectral estimate or spectrum. The periodogram [27]
is a tool to handle Fourier outputs, facilitating the detection and assessment of obvious and hidden
periodicities in time series operatively.
Time series of field observations gathered through history have been a significant source of
information, mainly in agriculture, providing empirical qualitative knowledge on past climates, trends
and societal impacts [33,34]. More recently, several authors have shown the potential of spectral analysis
for assessing periodic patterns and relationship with climatic drivers in reproductive phenology, from
large data sets of flowering and fruiting dates in tropical regions at species level [35–38]. Specifically,
Bush et al. [37] simulated phenological data by varying the level of uncertainty in the time series,
finding that levels of confidence were higher when working with longer time series even in noisy
data sets.
Long time series of remote sensing (RS) vegetation indices (VI) at high temporal frequency provide
detailed information on vegetation dynamics at large scales facilitating the assessment of vegetation
seasonality in a confident manner. The Normalized Difference Vegetation Index (NDVI) [39], based on
the visible and near-infrared spectral bands, is the most commonly vegetation index used as a proxy of
vegetation biomass or production [40]. Currently, NDVI3g dataset provides the longest NDVI time
series with more than 30 years of data derived from the Advanced Very High Resolution Radiometer
Remote Sens. 2019, 11, 2497 3 of 21

(AVHRR) sensor on board of the National Oceanic and Atmospheric Administration’s (NOAA’s) Polar
Orbiting Environmental Satellites (POES) [41]. In spite of the limitations of NDVI that saturates in
well-vegetated areas [42] and the 1/12◦ coarse resolution, the length of these time series makes it very
valuable for vegetation studies [43–46].
Common approaches to assess vegetation dynamics and seasonality from RS time series rely
on estimating the timing of the pheno-phases (i.e., start, end and length of growing cycles) through
different methodologies [18,44,47,48]. The number of seasonal cycles has been estimated by identifying
the number of maxima over smoothed time series based on threshold values and their dates of
occurrence [49–54]. Other methodologies rely on time series similarities requiring the previous
establishment of reference time series with typical seasonal cycles [55,56]. The majority of vegetation
studies are mainly focus on the phenological events whereas certain characteristics of seasonality such
as amplitude or stability of the cycles are not widely studied.
Little literature exists on the application of Fourier analysis to assess vegetation seasonality from
RS VI indexes. Olsson and Eklundh [57] and Verhoef, Menenti, and Azzali [58] evaluated vegetation
dynamics in Africa and South America respectively. Menenti et al. [59] were able to separate different
agro-climatic zones in Africa and Andres, Salas, and Skole [60] and Moody and Johnson [61] derived
land cover classifications of Brazil and southern California respectively. Azzali and Menenti [62]
were able to map land units in southern Africa in terms of leaf bud burst phenology and could
correlate amplitude with an aridity index. In agricultural areas, Jakubauskas, Legates, and Kastens [63]
and Canisius, Turral, and Molden [64] could identified different crops and bimodal agriculture in
Kansas (USA) and in Asia. More recently, Fourier analysis has been used to assess periodicities in
natural processes such as fire seasonality [65] and the number of vegetation phenological cycles [66].
Palacios-Orueta et al. [67] used it to demonstrate the existence of a double cycle in the spectral shape
angle AS1 index within the growing season of a cotton crop.
All of these studies were focused at local and regional scales being the application at global
scale not fully exploited. In addition, most of them have been focused on identifying the number
of intra-annual cycles (i.e., uni- or bimodal patterns). However, the information regarding to the
significance of periodicities and pluri-annual cycles has not been taken into consideration.
We propose the periodogram as a powerful tool to identify periodic patterns as a type of
“fingerprint” for vegetation cycles improving our ability to study phenology-related-cycle-indicators
using the entire time series in a highly operative way. Given the easy implementation of spectral
analysis and the present high computing capabilities, this methodology could be a valuable tool to
complement other approaches when assessing vegetation dynamics and seasonality from RS time series.
The objective of this work is to generate maps containing quantitative information of periodic
vegetation patterns (i.e., seasonality and pluri-annual cycles) at global scale from 1982 to 2016 using
NDVI3g data set. The specific objectives are the following:
(1) To map the number of intra-annual cycles;
(2) To map the amplitude and the stability of the seasonal cycles;
(3) To assess the presence of pluri-annual cycles taking advantage of the NDVI3g data set length;
(4) To assess the periodicity indicators developed according to the different bioclimates.

2. Materials and Methods

2.1. Remote Sensing Data

The dataset used was the Normalized Difference Vegetation Index-3rd generation version 1.1
(NDVI3g v1.1), derived from the Advanced Very High Resolution Radiometer (AVHRR) instrument
onboard the series of the National Oceanic and Atmospheric Administration (NOAA) satellites. It is
provided by NASA and compiled by the Global Inventory Monitoring and Modeling System (GIMMS)
project [41]. The scenes correspond to fortnightly composites with 1/12◦ spatial resolution. This dataset
provides the longest NDVI time series covering the Earth terrestrial surface enabling the extension of
Remote Sens. 2019, 11, 2497 4 of 21

the analysis to the early 1980s. It contains simple quality flags associated with NDVI values informing
on the retrieval process in case of low quality NDVI data. Thus, flag 0 indicates high quality NDVI
whereas flag 1 and 2 indicate low quality NDVI, retrieving values from spline interpolation or from
seasonal profile respectively.
In this study, negative values were masked with zero and missing values were replaced with
average values of the previous and next observations. The most of negative and missing values
are located at very high latitudes in the northern hemisphere (higher than 60 N) in winter and in
the Antarctica. The study period comprises from January 1982 to December 2016 constituting 840
global scenes.

2.2. Bioclimates Map

The bioclimates dataset was obtained from the climate regime classification used for mapping
the global ecological land units developed by the U.S. Geological Survey and Esri, published by the
Association of American Geographers (AAG) [68]. This classification consists of 37 bioclimates based
on the temperature and moisture regimes. It was provided at 250 meters spatial resolution in raster
format and resampled to 1/12◦ in order to reconcile with the NDVI dataset. Figure 1a shows the global
spatial distribution of the different bioclimates and Figure 1b shows the percentage of the number
of pixels within each bioclimate, indicating their representativeness at global scale and within the
thermal regime. Bioclimates under “very cold” and “cold” conditions present more pixels in wetter
regimes, particularly in the subclass “wet” whereas “hot” and “very hot” bioclimates show pixels
homogeneously distributed among water classes.

2.3. Precipitation Data

Monthly precipitation data from 1982 to 2015 and 0.5◦ spatial resolution were obtained freely
from the Climate Research Unit (CRU), version TS4 [69]. This dataset was used to assess the influence
of the precipitation annual distribution on the number of intra-annual cycles in water limited areas.
Remote Sens. 2019, 11, 2497 5 of 21
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Figure 1. (a) Bioclimates derived from the global ecological land units map [68]. The lighter and darker
colors indicate drier and more humid bioclimates respectively. (b) The number of pixels in percentage
Figure 1. (a) Bioclimates derived from the global ecological land units map [68]. The lighter and
per bioclimate.
darker colors indicate drier and more humid bioclimates respectively. (b) The number of pixels in
2.4. NDVI percentage
Spectral Analysis: Periodogram
per bioclimate.
Determination of the seasonal dynamics present in each NDVI time series was carried out by
means 2.4.
ofNDVI
classical Spectral Analysis:
spectral Periodogram
analysis [32,70,71]. More precisely seasonality was determined by the
estimationDetermination
of the respective periodograms that allowed
of the seasonal dynamics us to
present in identify
each NDVI the time
most series
significant periodicout by
was carried
components of each NDVI time series.
means of classical spectral analysis [32,70,71]. More precisely seasonality was determined by the
Periodogram
estimation ofisthe based on the classical
respective mathematical
periodograms theory
that allowed usoftoFourier
identify series. In a significant
the most Fourier series,
periodic
the signal is decomposed into a series
components of each NDVI time series. of sine and cosine waves at different frequencies called Fourier
frequencies (fi ). Thus, the
Periodogram is Fourier
based ontransform decomposition
the classical mathematical of the of xFourier
series
theory t is [70]:series. In a Fourier series,
the signal is decomposed into a X m
series of sine and cosine waves at different frequencies called Fourier
Xt = a0 + [ai · cos(2π fi t) + bi · sin(2π fi t)] + et (1)
frequencies (fi). Thus, the Fourier transform decomposition of the series xt is [70] :
i=1

where 𝑋 =𝑎 + [𝑎 ∙ cos 2𝜋𝑓 𝑡 + 𝑏 ∙ sin 2𝜋𝑓 𝑡 ] + 𝑒 (1)

xt are the equally spaced time series data
twhere
is the time subscript, t = 1, 2, . . . , n
xt are the equally spaced time series data
n is the number of observations in the time series
t is the time subscript, t= 1,2,…,n
n is the number of observations in the time series
Remote Sens. 2019, 11, 2497 6 of 21

ai and bi are the Fourier coefficients; i = 1, 2, . . . , m

m is the number of frequencies: m = n/2 if n is even; m = (n − 1)/2 if n is odd
fi is the i-th Fourier frequency: fi = i/n
a0 is the mean term: a0 = x
et : error term

The importance of each frequency (fi ) for explaining the variance of time series is measured by the
periodogram amplitude at that specific frequency (Equation (2)).
n 2 
I ( fi ) = · ai + bi 2 (2)
2
Thus, the periodogram is plotted as I(fi ) versus fi for i = 1, 2, . . . , n/2 or (n − 1)/2. In this case,
NDVI periodograms have 420 frequencies which is the half of the total time series observations.
A relatively large (small) value of I(fi ) indicates more (less) variance explained respectively for the
frequency fi in the time series oscillation. Thus, the most important periodicities are associated with
high amplitudes and vice versa. After an exploratory analysis at global scale, the highest amplitudes
were identified mainly at periods 24, 12 and 8, being considered as reference periods in this paper.
They correspond to the presence of a cycle every 24, 12 and 8 AVHRR periods representing annual,
half year and four months-terms respectively.
The seasonality significance was evaluated by means of the Fisher’s Kappa test (FK) [71] for the
periodogram. The statistic for this test is computed as the ratio between the maximum amplitude
value and the mean of all amplitudes according to the following equation 3:

max(I ( fi ))·m
FK = Pm (3)
i = 1 I ( fi )

The null hypothesis herein is that time series is white noise. The critical value for rejecting the
null hypothesis at the 1% significance level is 10.53. Pixels with time series considered as white noise
were removed for further analysis.
The NDVI periodogram was computed at pixel level using the “Genecycle” package [72] within R
environment software [73].

2.5. Periodicity Indicators

In order to assess the main patterns of the vegetation dynamics at global scale, four periodicity
indicators based on the spectral analysis of NDVI time series were defined: The seasonality mode (SM),
amplitude (SA) and stability (SS) regarding to the intra-annual cycles and an indicator related to the
relevance of pluri-annual cycles (PC) (Table 1). Note that the amplitudes at most higher periods are
not included in these indicators because their relationship with abrupt changes in time series either by
strong alterations in vegetation cover due to disturbances (e.g., fires, deforestation or flooding) or even
errors in the time series.
Figure S1 displays several examples of NDVI time series and their periodograms of different
ecosystem types and Table S1 shows the values of the seasonality indicators. The locations are shown
in Figure S2.
Remote Sens. 2019, 11, 2497 7 of 21

Table 1. Periodicity indicators for NDVI time series.

Indicator Statistical Computation Interpretation

Seasonality The period of the maximum amplitude (i.e., It indicates the occurrence of one,
Intra-annual cycles

Mode (SM) 24, 12 or 8) two or three intra-annual cycles.

The value of the maximum amplitude (i.e., at High values indicate high
Seasonality
24, 12 or 8 periods). The values range from 0 amplitude of the NDVI cycle at
Amplitude (SA)
to 100. the dominant seasonality mode.
Ratio between the value of the maximum
High values indicate high stability
amplitude (i.e., at 8, 12 or 24 periods) and the
Seasonality of a certain seasonality mode.
sum of the amplitudes at periods lower than
Stability (SS) Low values indicate a mix of
or equal to 24 (annual term). Values are in
seasonality modes.
percentage ranging between 0 and 100.
Ratio between the sum of all the amplitude It represents the variance
values between period 24 (one year) and explained by the pluri-annual
Pluri-annual
period 120 (5 years) and the sum of all the oscillations, from one to five-year
cycles (PC)
amplitudes. Values are in percentage ranging cycles. High values indicate the
between 0 and 100. presence of pluri-annual cycles.

3. Results

3.1. Global Vegetation Seasonality Mode

Three main types of seasonality stood out for their high ordinate values at 24, 12 and 8 AVHRR
periods indicating the presence of one, two and three intra-annual cycles respectively. The geographic
distribution of the predominant seasonality mode is shown in a three-color composition map (Figure 2a).
Pixels with a clear dominance of one (93.18%), two (4.43%) and three (1.15%) intra-annual seasonal
cycles are displayed in green, blue and red for the global land surface, with brighter colors indicating
high statistical significance. Only 1.24% of the total land surface, the FK test was not significant (less
than 10.53), suggesting the presence of areas with lack of seasonality in South America, Australia, and
Central Asia (Figure S3). Most of the areas with two and three intra-annual cycles are distributed
among “warm” to “very hot” bioclimates for all water regimes (tropical and arid areas) as well as in
agricultural areas (Figure 2b).
Remote Sens. 2019, 11, 2497 8 of 21
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a)

b)

Figure 2. (a) Spatial distribution of the three seasonality modes in an RGB color composition.
Figure 2. (a) Spatial distribution of the three seasonality modes in an RGB color composition. (b)
(b) Proportion of each type seasonality mode within bioclimates. Green, blue and red colors represent
Proportion of each type seasonality mode within bioclimates. Green, blue and red colors represent
ecosystems with one, two and three intra-annual cycles.
ecosystems with one, two and three intra-annual cycles.
3.2. Periodic Vegetation Patterns and Bioclimates: Relationship with the Main Climatic Drivers
3.2. Periodic Vegetation Patterns and Bioclimates: Relationship With the Main Climatic Drivers
Global maps of the NDVI SA, SS and PC values including the three seasonality modes are shown
Global
in Figure 3a–cmaps of the NDVI
respectively. SA, greater
SA values SS and than
PC values including
20 are located the three
primarily northseasonality modeswith
to the 50 parallel are
shown in Figures 3a, b and c respectively. SA values greater than 20 are located
some fluctuations depending probably on climate and orography. South to the latitude 50N, SA values primarily north to
the 50 parallel with some fluctuations depending probably on climate and orography.
decrease, reaching the lowest values in arid regions followed by tropical areas. Vegetation in mid and South to the
latitude
high 50N, of
latitudes SAthevalues decrease,
northern reaching
hemisphere showstheSS lowest
valuesvalues
higherinthan
arid60.regions followed
These regions by tropical
together with
areas. Vegetation in mid and high latitudes of the northern hemisphere shows
the African savannas show the highest stability patterns. Although lowest values are located in some SS values higher than
60.the
of These
aridregions
areas, sometogether with such
drylands the African savannas
as the Sahara show
Desert thestable
show highest stabilityTropical
patterns. patterns. Although
forests show
lowest values are located in some of the arid areas, some drylands such as
the lowest SS values in the Amazonian region. Lowest occurrence of pluri-annual cycles is observed the Sahara Desert show
at
stable patterns.
latitudes higher thanTropical forests
50 N and show
in the the savannas
African lowest SS valuesthe
whereas in highest
the Amazonian
values are region.
located inLowest
some
occurrence
arid areas. of pluri-annual cycles is observed at latitudes higher than 50 N and in the African
savannas
Figureswhereas
4–6 show the highest values
the boxplots of are
the located
SA, SS andin some arid areas.across the range of bioclimates for
PC indicators
Figures 4, 5 and 6 show the boxplots of the SA,
the three different SM (e.g., one, two and three intra-annual cycles). SS and PC Toindicators acrossofthe
easy inspection the range
boxplotsof
bioclimates
the bioclimatesforwere
the ordered
three different
firstly bySM (e.g. regime
thermal one, twoandand threebyintra-annual
secondly water classes, cycles). To easy
being removed
inspection of the boxplots the bioclimates were ordered firstly by thermal regime and secondly by
water classes, being removed from the analysis those bioclimates with none or few pixels. Similar
Remote Sens. 2019, 11, 2497 9 of 21

from the analysis those bioclimates with none or few pixels. Similar patterns of the SA, SS and PC were
observed independently of the number of intra-annual cycles. In general terms there is a significant
difference in seasonal amplitude (Figures 4a, 5a and 6a) between “very cold” to “cool” (values around
40) and “warm” to “very hot” bioclimates (values around 15) with higher values and larger within-class
variability of all water classes in the former case. Seasonality stability (Figures 4b, 5b and 6b) shows
high values (around 80) in “very cold” and “cold” bioclimates with low variability within water classes
and between thermal regimes. Higher amplitude and stability values are observed in the “wet”,
“moist” and “semi-dry” conditions across bioclimates from “cool” to “very hot”. “Very wet” classes
show low amplitude and stability and “dry” regimes show also low values, even lower than “very
dry” regimes. Pluri-annual cycles (Figures 4c, 5c and 6c) are mainly observed under water-limited
conditions (i.e., from “semi-dry” to “very dry” water classes) from “warm” to “very hot” thermal
regimes and with higher values in “dry” than in “very dry” conditions.
Amplitude and stability values are lower in regions with two intra-annual cycles while
pluri-annual cycles show similar values. Areas with three intra-annual cycles show lower values in the
three indicators.
Remote Sens. 2019, 11, 2497 10 of 21
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Figure 3. (a) Seasonality amplitude, (b) seasonality stability and (c) pluri-annual cycles indicator of
Figure 3. (a) Seasonality amplitude, (b) seasonality stability and (c) pluri-annual cycles indicator of
NDVI time series.
NDVI time series.
 Remote Sens. 2019, 11, 2497 11 of 21
Remote Sens. 2019, 11, x FOR PEER REVIEW 11 of 21

Figure 4. (a) Boxplots

Figure 4.of(a)
theBoxplots
seasonality amplitude,
of the (b) amplitude,
seasonality seasonality (b)
stability (c) andstability
seasonality the pluri-annual cycles
(c) and the indicator of
pluri-annual ecosystems
cycles with
indicator unimodal seasonal
of ecosystems with pattern per
each bioclimate. unimodal seasonal pattern per each bioclimate.
 Remote Sens. 2019, 11, 2497 12 of 21
Remote Sens. 2019, 11, x FOR PEER REVIEW 12 of 21

Figure 5. (a) Figure

Boxplots
5. of
(a)the seasonality
Boxplots of theamplitude,
seasonality(b) seasonality
amplitude, (b)stability (c) and
seasonality the pluri-annual
stability (c) and the cycles indicator
pluri-annual of ecosystems
cycles with
indicator of bimodal seasonal
ecosystems with pattern per
each bioclimate. bimodal seasonal pattern per each bioclimate.
 Remote Sens. 2019, 11, 2497 13 of 21
Remote Sens. 2019, 11, x FOR PEER REVIEW 13 of 21

Figure 6.of(a)
Figure 6. (a) Boxplots theBoxplots of the
seasonality
amplitude, (b) amplitude,
each bioclimate.
seasonality
seasonality (b) seasonality
stability (c) andstability (c) and the
the pluri-annual pluri-annual
cycles indicatorcycles indicatorwith
of ecosystems of ecosystems with pattern per
trimodal seasonal
trimodal seasonal pattern per each bioclimate.
Remote Sens. 2019, 11, 2497 14 of 21

4. Discussion
Useful indicators of vegetation dynamics were derived from NDVI time series by means of
periodogram, extracting information related to the number, amplitude and stability of intra-annual
cycles as well as the relevance of pluri-annual cycles. Throughout this discussion, the main periodic
vegetation patterns across bioclimates together with the possible driving factors were commented.
Due to the low spatial resolution of the data, this work is mainly focus on the relationship between
periodic vegetation patterns and climate. Only agricultural areas with a distinct seasonal pattern
were commented.
Most of the global vegetated land surface showed a single seasonal cycle with different values
of amplitude, stability and pluri-annual cycles (Figures 2a and 3). Vegetation with double and
triple intra-annual cycles showed a consistent spatial distribution, most of them located in arid and
tropical regions as well as in agricultural areas. These areas are coincident with those where several
authors found difficulties to identify phenological events due to the existence of multiple growing
seasons [74,75].
Areas with unimodal seasonality and high amplitude are mainly distributed in the circumpolar
region corresponding to climates from “very cold” to “cool” (Figure 4a). This pattern result from the
short growing season together with the large difference between vegetation and snow NDVI values [76].
In these areas, vegetation dynamics show highly stable intra- and inter-annual patterns specially
in the “very cold” and “cold” climates (Figure 3b–c), resulting probably from the low inter-annual
variability of temperature and illumination as main climatic constraints for vegetation growth in these
regions [77,78]. Other studies based on phenometric approach have shown similar results with low
variability in greenness onset and/or end of senescence [79] and length of growing season [80].
Higher amplitude values in boreal forest than in tundra ecosystem (Figure S1(1,2) and Table S1)
indicate that spatial variability in these regions may be related to land cover type, this is shown in a
consistent belt of boreal forest around 60–65 N that crosses latitudinally Eurasia and North America
(blue in Figure 3a). Verger et al. [81] found similar results in Eurasia but not in North America where
high values of Leaf Area Index (LAI) amplitude were located in the eastern part of the continent.
In climates from “warm” to “very hot”, amplitude is consistently low while the rest of the
indicators show high variability. In general terms, across temperature regimes lower stability values
are observed in the “very wet” and “dry” classes (Figures 4–6).
Within the arid regions (“dry” and “very dry” classes), extremely low amplitude of the seasonal
cycles must be due to NDVI low values throughout the year. Due to this reason, other authors
found difficulties in characterizing the seasonal cycles using a phenometric method [25,82] and others
exclude these areas from their studies [25,77,81,83] resulting in a lack of information about these areas.
The variability found in the rest of the indicators suggest that they contain relevant information to
assess vegetation dynamics in many arid regions of the world. This open new ways to evaluate more
accurately local patterns of vegetation dynamics derived from water availability at different scales due
to climatic patterns, atmosphere-land surface interactions and soil water retention capacity among
other reasons [84,85]. To illustrate the potential of the indicators, we present some of our findings in
several arid regions: (1) The Sahara Desert, (2) the Rub-al Khali Desert (Arabian Peninsula), (3) the
Sahel and (4) the Australian deserts.
The Sahara Desert shows a clear dominant unimodal pattern with high spatial variability of the
stability indicator (Figure 3b, Figure S1-5 and Table S1). Geomorphological features seem to have
a significant influence with higher SS located in high elevation areas (e.g., the Tibesti and Ahaggar
Mountains) whereas flat areas showed lower SS values. Rocky regions are able to maintain soil moisture
for longer periods than adjacent areas favoring vegetation growth. The influence of geomorphological
features on land surface phenology by controlling soil moisture has already been reported by other
authors [82].
The Rub’Al Khali Desert (a sand desert in the Arabian Peninsula) shows a trimodal seasonal pattern
(three intra-annual greening cycles) with consistent spatial distribution but low stability (Figures 2a
Remote Sens. 2019, 11, 2497 15 of 21

and 3b). While in this region the precipitation is extremely low and irregular, the periodogram analysis
has revealed also three intra-annual cycles due to probably to the occurrence of precipitation events
throughout the year (Figure S4). Our results indicate that water availability in sandy soils at specific
moments may trigger a fast vegetation response resulting in several short greening periods [86].
In addition, three intra-annual cycles were found in the Sahel area in a narrow band less than
100 km wide around latitude 15 N (Figure 2a, Figure S1-4 and Table S1). The presence of this pattern is
statistically significant and shows a high spatial coherence. Other authors mapped this area based on
other criteria such as NDVI threshold values [87] and precipitation amount [88]. However, the trimodal
pattern found in this work has not been identified in previous studies [54,81]. As in the Rub’Al Khali
desert, the periodogram of the precipitation suggests also three intra-annual cycles (Figure S5). Other
reasons for this pattern could be: (1) The presence of dry spells within a single rainy season between
July and October [89,90], (2) the coexistence of species with different phenological patterns and mixed
pixels [91] and (3) the presence data artifacts.
Near to random greening dynamics in large regions of Australian drylands accounted for 30% of
the pixels with statistically non-significant seasonality (Figure S1-6, Table S1 and Figure S3). In the
remaining area, seasonality stability is low and the occurrence of pluri-annual cycles high (Figure 6b,c).
This is in agreement with the intra- and inter-annual variability found in phenological events due to
irregularity of precipitation patterns [83,92].
A consistent bimodal seasonality pattern in the Horn of Africa, as well as Southern United States
and Northwestern Mexico responds to the existence of two rainy seasons (Figure 2a, Figure S1-3 and
Table S1). The displacement of the ITCZ in the one case [48] and the North American Monsoon in the
other [93] seems to have a significant impact in the vegetation seasonality.
In the evergreen broadleaf forest in Equatorial regions, the small seasonal amplitude found
(Figure 3a) is probably due to the permanent vegetation cover with subtle NDVI variations through the
year. The main climatic drivers that condition the seasonal dynamics in these regions have been subject
of controversy [78]. While some authors reported that greenness is higher during dry season [94],
others proposed that the vegetation index seasonality could be determined by the dormancy of the
forest in the dry periods [54].
In this work large areas with statistically significant and stable double seasonal pattern were found
in Africa responding to the displacement of the ITCZ [17,95,96]. Guan et al. [17] also found a double
cycle in Congo basin using Fourier spectrum of SEVERI LAI time series. In contrast, Vrieling et al. [54]
and Adole et al. [48] could not identify this pattern; however they found a double pattern in the Gulf
of Guinea using a phenometric approach.
Most of the Amazon basin showed one seasonal cycle which agrees with the results presented by
other authors [94]. The seasonality is characterized by a lower stability and a less consistent spatial
pattern than in Africa (Figure 3b, Figure 4b). “Very wet” bioclimates close to the equator showed
the lowest stability values resulting even in non-significant seasonality (Figure S3, Figure S1-8, and
Table S1). It has been shown previously that high cloudiness in the Amazon basin in wet seasons result
in many satellite corrupted observations [97,98] and high noise level in the vegetation indices time
series, making difficult to capture low variations in evergreen vegetation [25,74]. Our results indicate
that the presence of cloudiness may be a significant factor functioning on top of the canopy seasonal
dynamics and resulting in the low stability values observed. The presence of a double cycle together
with cloudiness artifacts is in agreement with the difficulty found when assessing phenological events
in these areas [74,75]. In addition, the high spatial heterogeneity in the seasonality stability indicator
may indicate the occurrence of land use changes resulting in a high seasonal variability at local scale.
Disturbances and anthropogenic processes also modify NDVI temporal patterns [99]. Agricultural
intensification with multiple cropping systems produces a strong modification on natural vegetation
seasonality and NDVI dynamics. Two intra-annual cycles were clearly identified in large rice
plantations of China, India, the Nile Delta and Southern Vietnam as previously reported by other
Remote Sens. 2019, 11, 2497 16 of 21

authors [54,64,100–102]. These results show the capacity of the periodogram derived indicators to
identify hot spots of high agriculture intensification.
In this work, we have assessed quantitatively a large variety of NDVI periodic patterns across
bioclimates. The northern regions limited by temperature and radiation show stable seasonality, while
in the water limited areas vegetation dynamics is highly variable within and between years, with
areas showing even a lack of statistically significant seasonality. Geomorphological features and the
variability of precipitation events are the main reasons. In particular, it has been possible to identify
consistent areas with a trimodal pattern maybe due to the fast response of vegetation to precipitation
events. In addition, it has been shown that cloudiness has a significant effect in the NDVI dynamics.
This information provides a better understanding of vegetation dynamics in terms of seasonality
and pluri-annual cycles that could be used as complementary information in vegetation phenology
studies. In this sense, the number of intra-annual cycles and stability could be used to parameterize
the models and assess the accuracy of the results.

5. Conclusions
The use of periodogram derived indicators has shown to be an operative and robust methodology
to assess global NDVI time series enabling to describe the Terrestrial Biosphere in terms of periodic
vegetation patterns, even in those regions with noisy or low NDVI values.
Although GIMMS NDVI3g dataset has been frequently used, this is the first time that it has been
analyzed using spectral analysis at global scale. Furthermore, the length of the time series with more
than 30 years of observations provided high power and robustness to the analysis.
The seasonality indicators (number, amplitude and stability) and pluri-annual cycles have shown
distinct patterns across bioclimates. The most important findings were the following:
(1) In the circumpolar regions, vegetation showed highly stable seasonality with a clear unimodal
pattern and high amplitude.
(2) Large areas with unimodal and bimodal patterns were identified in equatorial rainforest of
Africa and America respectively with higher stability in Africa. Not significant seasonality was found
in very wet areas in the Amazon Basin maybe due to cloudiness.
(3) Large semi-arid areas in Australia showed near to random seasonality patterns, linked probably
to the high precipitation variability. Also, pluri-annual cycles were identified.
(4) Three intra-annual cycles were found in Sahel region and the Arabian Peninsula suggesting a
vegetation synchrony with precipitation events.
(5) In the Sahara Desert high spatial variability in seasonality stability was found probably due to
different geomorphological features.
The availability of the information provided open new research paths in the context of vegetation
dynamics. This methodology is operative and could be implemented with other data sets at better
spatial resolution. Within the context of climate change, global warming and the increase of human
population, this would facilitate future management and conservation policies.

Supplementary Materials: The following are available online at http://www.mdpi.com/2072-4292/11/21/2497/s1,

Figure S1: NDVI time series (green) and their periodograms (blue) of different ecosystems. Locations in Figure S2.
Figure S2: The red dots are the locations of selected sites for detailed examination of NDVI time series and
periodograms. Figure S3: Spatial distribution of locations with non-significant seasonality (in red). Figure S4: (a)
Seasonality mode of NDVI and (b) precipitation time series in the Arabian Peninsula. Figure S5: (a) Seasonality
mode of NDVI and (b) precipitation time series in the Sahel area. Table S1: Seasonality indicators derived from
periodograms of NDVI time series from the locations of Figure S2.
Author Contributions: Conceptualization, L.R., J.L. and A.P.-O.; Data curation, J.E.P.; Formal analysis, L.R., and
J.L.; Investigation, L.R., J.L., J.E.P., M.H., M.C.M. and A.P.-O.; Methodology, L.R., J.L. and A.P.-O.; Software,
L.R. and J.L.; Visualization, L.R., J.E.P., M.H., M.C.M. and A.P.-O.; Writing—original draft, L.R. and A.P.-O.;
Writing—review & editing, L.R., J.L., J.E.P., M.H., M.C.M. and A.P.-O.
Funding: This research was funded by the Spanish Ministry of Science, Innovation and Universities through the
pre-doctoral grant of Laura Recuero [FPU014/05633].
Remote Sens. 2019, 11, 2497 17 of 21

Acknowledgments: We would like to thank NASA for providing the NDVI3g dataset and to the anonymous
reviewers for their valuable comments.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Chapin, F.S. Effects of plant traits on ecosystem and regional processes: A conceptual framework for
predicting the consequences of global change. Ann. Bot. 2003, 91, 455–463. [CrossRef] [PubMed]
2. Jax, K. Ecosystem Functioning; Cambridge University Press: Cambridge, UK, 2010; ISBN 978-0-521-70523-3.
3. Jax, K.; Jones, C.G.; Pickett, S.T.A. The Self-Identity of Ecological Units. Oikos 1998, 82, 253–264. [CrossRef]
4. Hylleberg, S. General Introduction. In Modelling seasonality; Hylleberg, S., Ed.; Oxford University Press:
Oxford, UK, 1992; pp. 3–14, ISBN 9780198773184.
5. Beveridge, W.H. Wheat Prices and Rainfall in Western Europe. J. R. Stat. Soc. 1922, 85, 412–475. [CrossRef]
6. Wood, C.A.; Lovett, R.R. Rainfall, drought and the solar cycle. Nature 1974, 251, 594–596. [CrossRef]
7. Feldstein, S.B.; Franzke, C.L.E. Atmospheric Teleconnection Patterns. In Nonlinear and Stochastic Climate
Dynamics; Franzke, C.L.E., O’Kane, T.J., Eds.; Cambridge University Press: Cambridge, UK, 2017; pp. 54–104.
8. Bartomeus, I.; Ascher, J.S.; Wagner, D.; Danforth, B.N.; Colla, S.; Kornbluth, S.; Winfree, R. Climate-associated
phenological advances in bee pollinators and bee-pollinated plants. Proc. Natl. Acad. Sci. USA 2011, 108,
20645–20649. [CrossRef]
9. Visser, M.E.; Noordwijk, A.V.; Tinbergen, J.M.; Lessells, C.M. Warmer springs lead to mistimed reproduction
in great tits (Parus major). Proc. R. Soc. B Biol. Sci. 1998, 265, 1867–1870. [CrossRef]
10. Renner, S.S.; Zohner, C.M. Climate Change and Phenological Mismatch in Trophic Interactions Among
Plants, Insects, and Vertebrates. Annu. Rev. Ecol. Evol. Syst. 2018, 49, 165–182. [CrossRef]
11. Mayor, S.J.; Guralnick, R.P.; Tingley, M.W.; Otegui, J.; Withey, J.C.; Elmendorf, S.C.; Andrew, M.E.; Leyk, S.;
Pearse, I.S.; Schneider, D.C. Increasing phenological asynchrony between spring green-up and arrival of
migratory birds. Sci. Rep. 2017, 7, 1902. [CrossRef]
12. Kharouba, H.M.; Ehrlén, J.; Gelman, A.; Bolmgren, K.; Allen, J.M.; Travers, S.E.; Wolkovich, E.M. Global
shifts in the phenological synchrony of species interactions over recent decades. Proc. Natl. Acad. Sci. USA
2018, 115, 5211–5216. [CrossRef]
13. Tucker, C.J.; Fung, I.Y.; Keeling, C.D.; Gammon, R.H. Relationship between atmospheric CO2 variations and
a satellite-derived vegetation index. Nature 1986, 319, 195–199. [CrossRef]
14. Keeling, C.D.; Chin, J.F.S.; Whorf, T.P. Increased activity of northern vegetation inferred from atmospheric
CO2 measurements. Nature 1996, 382, 146–149. [CrossRef]
15. McPherson, R.A. A review of vegetation-atmosphere interactions and their influences on mesoscale
phenomena. Prog. Phys. Geogr. 2007, 31, 261–285. [CrossRef]
16. Richardson, A.D.; Keenan, T.F.; Migliavacca, M.; Ryu, Y.; Sonnentag, O.; Toomey, M. Climate change,
phenology, and phenological control of vegetation feedbacks to the climate system. Agric. For. Meteorol.
2013, 169, 156–173. [CrossRef]
17. Guan, K.; Medvigy, D.; Wood, E.F.; Caylor, K.K.; Li, S.; Jeong, S.J. Deriving vegetation phenological time and
trajectory information over africa using seviri daily LAI. IEEE Trans. Geosci. Remote Sens. 2014, 52, 1113–1130.
[CrossRef]
18. Zhang, X.; Friedl, M.A.; Schaaf, C.B.; Strahler, A.H.; Hodges, J.C.F.; Gao, F.; Reed, B.C.; Huete, A. Monitoring
vegetation phenology using MODIS. Remote Sens. Environ. 2003, 84, 471–475. [CrossRef]
19. Zhu, J.; Zeng, X. Influences of the seasonal growth of vegetation on surface energy budgets over middle to
high latitudes. Int. J. Climatol. 2017, 37, 4251–4260. [CrossRef]
20. Parmesan, C. Ecological and Evolutionary Responses to Recent Climate Change. Annu. Rev. Ecol. Evol. Syst.
2006, 37, 637–669. [CrossRef]
21. IPCC. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment
Report of the Intergovernmental Panel on Climate Change; Core Writing Team, Pachauri, R.K., Meyer, L.A., Eds.;
IPCC: Geneva, Switzerland, 2014; ISBN 978-92-9169-143-2.
22. Churkina, G.; Running, S.W. Contrasting Climatic Controls on the Estimated Productivity of Global Terrestrial
Biomes. Ecosystems 1998, 1, 206–215. [CrossRef]
Remote Sens. 2019, 11, 2497 18 of 21

23. Garonna, I.; de Jong, R.; Stöckli, R.; Schmid, B.; Schenkel, D.; Schimel, D.; Schaepman, M.E. Shifting relative
importance of climatic constraints on land surface phenology. Environ. Res. Lett. 2018, 13, 024025. [CrossRef]
24. Nemani, R.R.; Keeling, C.D.; Hashimoto, H.; Jolly, W.M.; Piper, S.C.; Tucker, C.J.; Myneni, R.B.; Running, S.W.
Climate-Driven Increases in Global Terrestrial Net Primary Production from 1982 to 1999. Science 2003, 300,
1560–1563. [CrossRef]
25. Zhang, X.; Friedl, M.A.; Schaaf, C.B. Global vegetation phenology from Moderate Resolution Imaging
Spectroradiometer (MODIS): Evaluation of global patterns and comparison with in situ measurements.
J. Geophys. Res. Biogeosci. 2006, 111, G04017. [CrossRef]
26. Walden, A.T.; Percival, D.B.; McCoy, E.J. Spectrum estimation by wavelet thresholding of multitaper
estimators. IEEE Trans. Signal Process. 1998, 46, 3153–3165. [CrossRef]
27. Schuster, A. On the investigation of hidden periodicities with application to a supposed 26 day period of
meteorological phenomena. J. Geophys. Res. 1898, 3, 13–41. [CrossRef]
28. Schuster, A. On the Periodicities of Sunspots. Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 1906, 206, 69–100.
[CrossRef]
29. Nawaz, S.; Khan, A.A.; Mahmood, A.; Javed, C.F. Performance Analysis of the Time-Based and
Periodogram-Based Energy Detector for Spectrum Sensing. Int. J. Electr. Comp. Energ. Electr. Commun. Eng.
2017, 11, 586–590.
30. Kayham, A.S.; El-Jaroudi, A.; Chaparro, L.F. Evolutionary Periodogram for Nonstationary Signals. IEEE Trans.
Signal Process. 1994, 42, 1527–1536. [CrossRef]
31. Zakharov, Y.V.; Baronkin, V.M.; Tozer, T.C. DFT-based frequency estimators with narrow acquisition range.
IEE Proc. Commun. 2001, 148, 1–7. [CrossRef]
32. Bloomfield, P. Fourier Analysis of Time Series: An Introduction, 2nd ed.; John Wiley & Sons: New York, NY,
USA, 2001; ISBN 0-471-88948-2.
33. Lieth, H. (Ed.) Phenology and Seasonality Modeling; Springer Science + Business Media: New York, NY, USA,
1974; ISBN 978-3-642-51865-2.

34. Van Vliet, A.J.H.; De Groot, R.S.; Bellens, Y.; Braun, P.; Bruegger, R.; Bruns, E.; Clevers, J.; Estreguil, C.;
Flechsig, M.; Jeanneret, F.; et al. The European Phenology Network. Int. J. Biometeorol. 2003, 47, 202–212.
[CrossRef]
35. Zalamea, P.C.; Munoz, F.; Stevenson, P.R.; Timothy Paine, C.E.; Sarmiento, C.; Sabatier, D.; Heuret, P.
Continental-scale patterns of Cecropia reproductive phenology: Evidence from herbarium specimens.
Proc. R. Soc. B Biol. Sci. 2011, 278, 2437–2445. [CrossRef]
36. Adamescu, G.S.; Plumptre, A.J.; Abernethy, K.A.; Polansky, L.; Bush, E.R.; Chapman, C.A.; Shoo, L.P.;
Fayolle, A.; Janmaat, K.R.L.; Robbins, M.M.; et al. Annual cycles are the most common reproductive strategy
in African tropical tree communities. Biotropica 2018, 50, 418–430. [CrossRef]
37. Bush, E.R.; Abernethy, K.A.; Jeffery, K.; Tutin, C.; White, L.; Dimoto, E.; Dikangadissi, J.T.; Jump, A.S.;
Bunnefeld, N. Fourier analysis to detect phenological cycles using long-term tropical field data and
simulations. Methods Ecol. Evol. 2017, 8, 530–540. [CrossRef]
38. Chapman, C.A.; Wrangham, R.W.; Chapman, L.J.; Kennard, D.K.; Zanne, A.E. Fruit and flower phenology at
two sites in Kibale National Park, Uganda. J. Trop. Ecol. 1999, 15, 189–211. [CrossRef]
39. Tucker, C.J. Red and photographic infrared linear combinations for monitoring vegetation.
Remote Sens. Environ. 1979, 8, 127–150. [CrossRef]
40. Baret, F.; Guyot, G. Potentials and limits of vegetation indices for LAI and APAR assessment.
Remote Sens. Environ. 1991, 35, 161–173. [CrossRef]
41. Pinzon, J.E.; Tucker, C.J. A non-stationary 1981-2012 AVHRR NDVI3g time series. Remote Sens. 2014, 6,
6929–6960. [CrossRef]
42. Huete, A.; Didan, K.; Miura, T.; Rodriguez, E.; Gao, X.; Ferreira, L. Overview of the radiometric and biophysical
performance of the MODIS vegetation indices. Remote Sens. Environ. 2002, 83, 195–213. [CrossRef]
43. Park, T.; Ganguly, S.; Tømmervik, H.; Euskirchen, E.S.; Høgda, K.A.; Karlsen, S.R.; Brovkin, V.; Nemani, R.R.;
Myneni, R.B. Changes in growing season duration and productivity of northern vegetation inferred from
long-term remote sensing data. Environ. Res. Lett. 2016, 11, 084001. [CrossRef]
Remote Sens. 2019, 11, 2497 19 of 21

44. White, M.A.; de Beurs, K.M.; Didan, K.; Inouye, D.W.; Richardson, A.D.; Jensen, O.P.; O’Keefe, J.; Zhang, G.;
Nemani, R.R.; van Leeuwen, W.J.D.; et al. Intercomparison, interpretation, and assessment of spring
phenology in North America estimated from remote sensing for 1982–2006. Glob. Chang. Biol. 2009, 15,
2335–2359. [CrossRef]
45. White, M.A.; Nemani, R.R. Real-time monitoring and short-term forecasting of land surface phenology.
Remote Sens. Environ. 2006, 104, 43–49. [CrossRef]
46. Yu, L.; Liu, T.; Bu, K.; Yan, F.; Yang, J.; Chang, L. Monitoring the long term vegetation phenology change in
Northeast China from 1982 to 2015. Sci. Rep. 2017, 7, 14770. [CrossRef]
47. Atzberger, C.; Klisch, A.; Mattiuzzi, M.; Vuolo, F. Phenological metrics derived over the European continent
from NDVI3g data and MODIS time series. Remote Sens. 2013, 6, 257–284. [CrossRef]
48. Adole, T.; Dash, J.; Atkinson, P.M. Characterising the land surface phenology of Africa using 500 m MODIS
EVI. Appl. Geogr. 2018, 90, 187–199. [CrossRef]
49. Ding, M.; Chen, Q.; Xiao, X.; Xin, L.; Zhang, G.; Li, L. Variation in cropping intensity in northern China from
1982 to 2012 based on GIMMS-NDVI data. Sustainability 2016, 8, 1123. [CrossRef]
50. Estel, S.; Kuemmerle, T.; Levers, C.; Baumann, M.; Hostert, P. Mapping cropland-use intensity across Europe
using MODIS NDVI time series. Environ. Res. Lett. 2016, 11, 024015. [CrossRef]
51. Jönsson, P.; Eklundh, L. Seasonality extraction by function fitting to time-series of satellite sensor data.
IEEE Trans. Geosci. Remote Sens. 2002, 40, 1824–1832. [CrossRef]
52. Kontgis, C.; Schneider, A.; Ozdogan, M. Mapping rice paddy extent and intensification in the Vietnamese
Mekong River Delta with dense time stacks of Landsat data. Remote Sens. Environ. 2015, 169, 255–269.
[CrossRef]
53. Sakamoto, T.; Van Nguyen, N.; Ohno, H.; Ishitsuka, N.; Yokozawa, M. Spatio-temporal distribution of rice
phenology and cropping systems in the Mekong Delta with special reference to the seasonal water flow of
the Mekong and Bassac rivers. Remote Sens. Environ. 2006, 100, 1–16. [CrossRef]
54. Vrieling, A.; De Leeuw, J.; Said, M.Y. Length of growing period over africa: Variability and trends from 30
years of NDVI time series. Remote Sens. 2013, 5, 982–1000. [CrossRef]
55. Guan, X.; Huang, C.; Liu, G.; Meng, X.; Liu, Q. Mapping rice cropping systems in Vietnam using an
NDVI-based time-series similarity measurement based on DTW distance. Remote Sens. 2016, 8, 19. [CrossRef]
56. Zhang, Y.; Hepner, G.F. The Dynamic-Time-Warping-based k -means++ clustering and its application in
phenoregion delineation. Int. J. Remote Sens. 2017, 38, 1720–1736. [CrossRef]
57. Olsson, L.; Eklundh, L. Fourier Series for analysis of temporal sequences of satellite sensor imagery. Int. J.
Remote Sens. 1994, 15, 3735–3741. [CrossRef]
58. Verhoef, W.; Menenti, M.; Azzali, S. Cover a colour composite of NOAA-AVHRR-NDVI based on time series
analysis (1981-1992). Int. J. Remote Sens. 1996, 17, 231–235. [CrossRef]
59. Menenti, M.; Azzali, S.; Verhoef, W.; van Swol, R. Mapping agroecological zones and time lag in vegetation
growth by means of fourier analysis of time series of NDVI images. Adv. Space Res. 1993, 13, 233–237.
[CrossRef]
60. Andres, L.; Salas, W.A.; Skole, D. Fourier analysis of multi-temporal AVHRR data applied to a land cover
classification. Int. J. Remote Sens. 1994, 15, 1115–1121. [CrossRef]
61. Moody, A.; Johnson, D.M. Land-Surface Phenologies from AVHRR Using the Discrete Fourier Transform.
Remote Sens. Environ. 2001, 75, 305–323. [CrossRef]
62. Azzali, S.; Menenti, M. Mapping vegetation-soil-climate complexes in southern Africa using temporal Fourier
analysis of NOAA-AVHRR NDVI data. Int. J. Remote Sens. 2000, 21, 973–996. [CrossRef]
63. Jakubauskas, M.E.; Legates, D.R.; Kastens, J.H. Crop identification using harmonic analysis of time-series
AVHRR NDVI data. Comput. Electron. Agric. 2002, 37, 127–139. [CrossRef]
64. Canisius, F.; Turral, H.; Molden, D. Fourier analysis of historical NOAA time series data to estimate bimodal
agriculture. Int. J. Remote Sens. 2007, 28, 5503–5522. [CrossRef]
65. Huesca, M.; Litago, J.; Palacios-Orueta, A.; Montes, F.; Sebastián-López, A.; Escribano, P. Assessment of
forest fire seasonality using MODIS fire potential: A time series approach. Agric. For. Meteorol. 2009, 149,
1946–1955. [CrossRef]
66. Vrieling, A.; Meroni, M.; Mude, A.G.; Chantarat, S.; Ummenhofer, C.C.; de Bie, K.C.A.J.M. Early
assessment of seasonal forage availability for mitigating the impact of drought on East African pastoralists.
Remote Sens. Environ. 2016, 174, 44–55. [CrossRef]
Remote Sens. 2019, 11, 2497 20 of 21

67. Palacios-Orueta, A.; Huesca, M.; Whiting, M.L.; Litago, J.; Khanna, S.; Garcia, M.; Ustin, S.L. Derivation of
phenological metrics by function fitting to time-series of Spectral Shape Indexes AS1 and AS2: Mapping
cotton phenological stages using MODIS time series. Remote Sens. Environ. 2012, 126, 148–159. [CrossRef]
68. Sayre, R.; Dangermond, J.; Frye, C.; Vaughan, R.; Aniello, P.; Breyer, S.; Cribbs, D.; Hopkins, D.; Nauman, R.;
Derrenbacher, W.; et al. A New Map of Global Ecological Land Units—An Ecophysiographic Stratification Approach;
Association of American Geographers: Washington, DC, USA, 2014; p. 46.
69. University of East Anglia Climatic Research Unit; Harris, I.C.; Jones, P.D. CRU TS4.00: Climatic Research Unit
(CRU) Time-Series (TS) Version 4.00 of High-Resolution Gridded Data of Month-by-Month Variation in Climate (Jan.
1901–Dec. 2015); Centre for Environmental Data Analysis: Didcot, UK, 2017.
70. Box, G.E.P.; Jenkins, G.M.; Reinsel, G.C. Time Series Analysis. Forecasting and Control, 3rd ed.; Prentice Hall:
Englewood Cliff, NJ, USA, 1994; ISBN 0-13-060774-6.
71. Fuller, W.A. Introduction to Statistical Time Series; John Wiley and Sons: New York, NY, USA, 1976.
72. Ahdesmaki, M.; Fokianos, K.; Strimmer, K. GeneCycle: Identification of Periodically Expressed Genes, R
package version 1.1.2. 2015; Available online: http:CRAN.R-project.org/package=GeneCycle (accessed on
1 August 2016).
73. R Core Team. R: A Language and Environment for Statistical Computing. Available online: http:
//www.r-project.org/ (accessed on 15 October 2018).
74. Maignan, F.; Bréon, F.M.; Bacour, C.; Demarty, J.; Poirson, A. Interannual vegetation phenology estimates
from global AVHRR measurements. Comparison with in situ data and applications. Remote Sens. Environ.
2008, 112, 496–505. [CrossRef]
75. Julien, Y.; Sobrino, J.A. Global land surface phenology trends from GIMMS database. Int. J. Remote Sens.
2009, 30, 3495–3513. [CrossRef]
76. Beck, P.S.A.; Atzberger, C.; Høgda, K.A.; Johansen, B.; Skidmore, A.K. Improved monitoring of vegetation
dynamics at very high latitudes: A new method using MODIS NDVI. Remote Sens. Environ. 2006, 100,
321–334. [CrossRef]
77. Zhang, X.; Tan, B.; Yu, Y. Interannual variations and trends in global land surface phenology derived from
enhanced vegetation index during 1982–2010. Int. J. Biometeorol. 2014, 58, 547–564. [CrossRef]
78. Forkel, M.; Migliavacca, M.; Thonicke, K.; Reichstein, M.; Schaphoff, S.; Weber, U.; Carvalhais, N. Codominant
water control on global interannual variability and trends in land surface phenology and greenness.
Glob. Chang. Biol. 2015, 21, 3414–3435. [CrossRef]
79. Rodriguez-Galiano, V.F.; Dash, J.; Atkinson, P.M. Characterising the land surface phenology of Europe using
decadal MERIS data. Remote Sens. 2015, 7, 9390–9409. [CrossRef]
80. De Jong, R.; de Bruin, S.; de Wit, A.; Schaepman, M.E.; Dent, D.L. Analysis of monotonic greening and
browning trends from global NDVI time-series. Remote Sens. Environ. 2011, 115, 692–702. [CrossRef]
81. Verger, A.; Filella, I.; Baret, F.; Peñuelas, J. Vegetation baseline phenology from kilometric global LAI satellite
products. Remote Sens. Environ. 2016, 178, 1–14. [CrossRef]
82. Yan, D.; Zhang, X.; Yu, Y.; Guo, W.; Hanan, N.P. Characterizing land surface phenology and responses to
rainfall in the Sahara desert. J. Geophys. Res. Biogeosci. 2016, 121, 2243–2260. [CrossRef]
83. Zhao, L.; Dai, A.; Dong, B. Changes in global vegetation activity and its driving factors during 1982–2013.
Agric. For. Meteorol. 2018, 249, 198–209. [CrossRef]
84. Schwinning, S.; Sala, O.E.; Loik, M.E.; Ehleringer, J.R. Thresholds, memory, and seasonality: Understanding
pulse dynamics in arid/semi-arid ecosystems. Oecologia 2004, 141, 191–193. [CrossRef] [PubMed]
85. Vicente-Serrano, S.M.; Gouveia, C.; Camarero, J.J.; Begueria, S.; Trigo, R.; Lopez-Moreno, J.I.;
Azorin-Molina, C.; Pasho, E.; Lorenzo-Lacruz, J.; Revuelto, J.; et al. Response of vegetation to drought
time-scales across global land biomes. Proc. Natl. Acad. Sci. USA 2013, 110, 52–57. [CrossRef] [PubMed]
86. Noy-Meir, I. Desert Ecosystems: Environment and Producers. Annu. Rev. Ecol. Syst. 1973, 4, 25–51.
[CrossRef]
87. Kim, D.; Chin, M.; Remer, L.A.; Diehl, T.; Bian, H.; Yu, H.; Brown, M.E.; Stockwell, W.R. Role of surface wind
and vegetation cover in multi-decadal variations of dust emission in the Sahara and Sahel. Atmos. Environ.
2017, 148, 282–296. [CrossRef]
88. Anyamba, A.; Small, J.L.; Tucker, C.J.; Pak, E.W. Thirty-two Years of Sahelian Zone Growing Season
Non-Stationary NDVI3g Patterns. Remote Sens. 2014, 6, 3101–3122. [CrossRef]
Remote Sens. 2019, 11, 2497 21 of 21

89. Anyamba, A.; Tucker, C.J. Analysis of Sahelian vegetation dynamics using NOAA-AVHRR NDVI data from
1981–2003. J. Arid Environ. 2005, 63, 596–614. [CrossRef]
90. Abdi, A.M.; Boke-Olén, N.; Tenenbaum, D.E.; Tagesson, T.; Cappelaere, B.; Ardö, J. Evaluating water controls
on vegetation growth in the semi-arid sahel using field and earth observation data. Remote Sens. 2017, 9, 294.
[CrossRef]
91. Brandt, M.; Hiernaux, P.; Tagesson, T.; Verger, A.; Rasmussen, K.; Diouf, A.A.; Mbow, C.; Mougin, E.;
Fensholt, R. Woody plant cover estimation in drylands from Earth Observation based seasonal metrics.
Remote Sens. Environ. 2016, 172, 28–38. [CrossRef]
92. Broich, M.; Huete, A.; Tulbure, M.G.; Ma, X.; Xin, Q.; Paget, M.; Restrepo-Coupe, N.; Davies, K.; Devadas, R.;
Held, A. Land surface phenological response to decadal climate variability across Australia using satellite
remote sensing. Biogeosciences 2014, 11, 5181–5198. [CrossRef]
93. Adams, D.K.; Comrie, A.C. The North American Monsoon. Bull. Amer. Meteor. Soc. 1997, 78, 2197–2213.
[CrossRef]
94. Myneni, R.B.; Yang, W.; Nemani, R.R.; Huete, A.R.; Dickinson, R.E.; Knyazikhin, Y.; Didan, K.; Fu, R.; Negron
Juarez, R.I.; Saatchi, S.S.; et al. Large seasonal swings in leaf area of Amazon rainforests. Proc. Natl. Acad.
Sci. USA 2007, 104, 4820–4823. [CrossRef] [PubMed]
95. Yan, D.; Zhang, X.; Yu, Y.; Guo, W.A. Comparison of Tropical Rainforest Phenology Retrieved from
Geostationary (SEVIRI) and Polar-Orbiting (MODIS) Sensors Across the Congo Basin. IEEE Trans. Geosci.
Remote Sens. 2016, 54, 4867–4881. [CrossRef]
96. Gond, V.; Fayolle, A.; Pennec, A.; Cornu, G.; Mayaux, P.; Camberlin, P.; Doumenge, C.; Fauvet, N.;
Gourlet-Fleury, S. Vegetation structure and greenness in Central Africa from Modis multi-temporal data.
Philos. Trans. R. Soc. B Biol. Sci. 2013, 368, 20120309. [CrossRef]
97. Hilker, T.; Lyapustin, A.I.; Tucker, C.J.; Hall, F.G.; Myneni, R.B.; Wang, Y.; Bi, J.; Mendes de Moura, Y.;
Sellers, P.J. Vegetation dynamics and rainfall sensitivity of the Amazon. Proc. Natl. Acad. Sci. USA 2014, 111,
16041–16046. [CrossRef]
98. Samanta, A.; Ganguly, S.; Vermote, E.; Nemani, R.R.; Myneni, R.B. Why Is Remote Sensing of Amazon Forest
Greenness So Challenging? Earth Interact. 2012, 16, 1–14. [CrossRef]
99. Evans, J.; Geerken, R. Discrimination between climate and human-induced dryland degradation.
J. Arid Environ. 2004, 57, 535–554. [CrossRef]
100. Chauhan, B.S.; Mahajan, G.; Sardana, V.; Timsina, J.; Jat, M.L. Productivity and Sustainability of the Rice-Wheat
Cropping System in the Indo-Gangetic Plains of the Indian Subcontinent: Problems, Opportunities, and
Strategies. In Advances in Agronomy, 1st ed.; Sparks, D.L., Ed.; Elsevier: Amsterdam, The Netherlands, 2012;
Volume 117, pp. 315–369, ISBN 978-0-12-394278-4.
101. Nguyen, T.T.H.; De Bie, C.A.J.M.; Ali, A.; Smaling, E.M.A.; Chu, T.H. Mapping the irrigated rice cropping
patterns of the Mekong delta, Vietnam, through hyper-temporal SPOT NDVI image analysis. Int. J.
Remote Sens. 2012, 33, 415–434. [CrossRef]
102. Kotb, T.H.S.; Watanabe, T.; Ogino, Y.; Tanji, K.K. Soil salinization in the Nile Delta and related policy issues
in Egypt. Agric. Water Manag. 2000, 43, 239–261. [CrossRef]

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