remote sensing

Article
Using Ordinary Digital Cameras in Place of
Near-Infrared Sensors to Derive Vegetation Indices
for Phenology Studies of High Arctic Vegetation
Helen B. Anderson 1 , Lennart Nilsen 1, *, Hans Tømmervik 2 , Stein Rune Karlsen 3 , Shin Nagai 4
and Elisabeth J. Cooper 1
1 Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics,
UiT: The Arctic University of Norway, NO-9037 Tromsø, Norway; helen.anderson@uit.no (H.B.A.);
elisabeth.cooper@uit.no (E.J.C.)
2 Norwegian Institute for Nature Research, FRAM-High North Centre for Climate and the Environment,
P.O. Box 6606 Langnes, NO-9296 Tromsø, Norway; hans.tommervik@nina.no
3 Norut Northern Research Institute, P.O. Box 6434, NO-9294 Tromsø, Norway; stein-rune.karlsen@norut.no
4 Department of Environmental Geochemical Cycle Research, Japan Agency for Marine-Earth Science
and Technology, Kanazawa-ku, 236-0001 Yokohama, Japan; nagais@jamstec.go.jp
* Correspondence: lennart.nilsen@uit.no; Tel.: +47-776-46314

Academic Editors: Randolph H. Wynne and Prasad S. Thenkabail

Received: 21 April 2016; Accepted: 8 October 2016; Published: 17 October 2016

Abstract: To remotely monitor vegetation at temporal and spatial resolutions unobtainable

with satellite-based systems, near remote sensing systems must be employed. To this extent
we used Normalized Difference Vegetation Index NDVI sensors and normal digital cameras
to monitor the greenness of six different but common and widespread High Arctic plant
species/groups (graminoid/Salix polaris; Cassiope tetragona; Luzula spp.; Dryas octopetala/S. polaris;
C. tetragona/D. octopetala; graminoid/bryophyte) during an entire growing season in central Svalbard.
Of the three greenness indices (2G_RBi, Channel G% and GRVI) derived from digital camera
images, only GRVI showed significant correlations with NDVI in all vegetation types. The GRVI
(Green-Red Vegetation Index) is calculated as (GDN − RDN )/(GDN + RDN ) where GDN is Green digital
number and RDN is Red digital number. Both NDVI and GRVI successfully recorded timings of the
green-up and plant growth periods and senescence in all six plant species/groups. Some differences
in phenology between plant species/groups occurred: the mid-season growing period reached a
sharp peak in NDVI and GRVI values where graminoids were present, but a prolonged period of
higher values occurred with the other plant species/groups. In particular, plots containing C. tetragona
experienced increased NDVI and GRVI values towards the end of the season. NDVI measured with
active and passive sensors were strongly correlated (r > 0.70) for the same plant species/groups.
Although NDVI recorded by the active sensor was consistently lower than that of the passive sensor
for the same plant species/groups, differences were small and likely due to the differing light sources
used. Thus, it is evident that GRVI and NDVI measured with active and passive sensors captured
similar vegetation attributes of High Arctic plants. Hence, inexpensive digital cameras can be used
with passive and active NDVI devices to establish a near remote sensing network for monitoring
changing vegetation dynamics in the High Arctic.

Keywords: NDVI; greenness index; RGB camera; vegetation; phenology; active sensor;
passive sensor; Svalbard

Remote Sens. 2016, 8, 847; doi:10.3390/rs8100847 www.mdpi.com/journal/remotesensing

Remote Sens. 2016, 8, 847 2 of 17

1. Introduction
Recording the changing phenology of vegetation has been a long term aim of many researchers
in efforts to understand ecosystem processes and the drivers of environmental change [1]. Direct
observations of phenological events have been collected by numerous individuals, sometimes over
many generations [2]. The vast majority of such data gathered so far comes from mid-latitude temperate
regions and has highlighted important shifts in phenology such as an advancement in the timing
of the onset of spring [3–5]. However, it has been argued that increased monitoring efforts should
focus on polar regions [6], particularly as these areas have experienced greater than global-average
increases in annual temperatures [7] and are intimately linked to other parts of the globe via complex
atmospheric and oceanic cycles [8,9]. Field-based manual phenological observations in Arctic, Antarctic
and alpine areas have been ongoing for a number of years at single sites [10,11] and multiple sites
through coordinated networks such as the International Tundra Experiment [12,13]. However such
traditional approaches can be problematic due to the time constraints imposed by short summer
periods, the highly labour-intensive nature of the work, high financial costs and difficulties in accessing
remote locations.
Technological advances in remote sensing however, have greatly assisted in monitoring remote
and difficult to access regions of the globe, such as polar regions, as well as enabling more rigorous
phenological data to be collected in greater detail [1]. In this respect, satellite imagery has provided
much data and opportunities for assessment of environmental change [14,15], particularly through
use of the Normalised Difference Vegetation Index (NDVI) [16]. The NDVI expresses the ratio of red
and near-infrared light absorbed and reflected by vegetation [17] and thus can be used as a proxy
measure for above-ground plant productivity and phenology [17,18]. Although NDVI is by far the
most popular vegetation index used [19,20], it is only one of a number of indices derived from visible
and near-visible wavelengths that can be employed to describe phenological change [21]. Indeed, the
use of indices derived from red, green and blue wavelengths are becoming more common [22,23],
particularly since the growing availability of relatively inexpensive digital cameras has increased
possibilities for in-situ field-based monitoring (near remote sensing [22]) of vegetation [1].
Near remote sensing using multispectral sensors offers the benefits of recording data at spatial
and temporal resolutions often unobtainable with satellite-based systems, whilst also overcoming the
problems associated with a lack of useable data collected by satellites during cloudy conditions and
from areas covered by shadows [23,24], solar geometry [25] and snow cover [26]. Near remote sensing
using digital cameras to track the phenological change of forest canopies and grasslands has taken place
at lower latitudes, with some assessment of the applicability of the vegetation indices used [22,27–30].
At higher latitudes, ordinary digital cameras have begun to be used to record phenological status or
other parameters of Arctic tundra vegetation [31,32], with the automation of such devices offering
obvious benefits for monitoring vegetation in these remote areas.
Existing studies of vegetation phenology in the Arctic have used digital cameras to capture
change at the habitat level, focussing on groups classed as fen, heath, copse and snowbed [31,32].
Here, we use near remote sensing to record plant greenness as an indication of phenological stage
in six different plant species/groups in the High Arctic during an entire growing season. In doing
so we make an assessment of the ability of different vegetation indices to monitor the greenness of
common and widespread High Arctic plants and describe differences in phenological development
and phenological stages (e.g., snowmelt, start of the growing season, max/peak of the growing season,
end of the growing season and first autumn snow fall) observed between species. Specifically, we have
addressed the following questions:

• Can different greenness indices derived from images captured by near remote sensing digital
cameras be used to reliably monitor the phenological cycle of separate High Arctic plant
species/groups, and which index best represents such changes?
 Remote Sens. 2016, 8, 847 3 of 17

Remote Sens. 2016, 8, 847 3 of 16

• How well correlated was the best performing greenness index, derived from digital camera
images, with NDVI data?
To answer these questions, we recorded the greenness of six High Arctic plant species/groups
• Can different near remote sensing NDVI devices reliably monitor the greenness of separate High
across an entire growing season using data collected from ordinary digital cameras and two different
Arctic plant species/groups, and how well correlated were the data gathered by these sensors?
NDVI sensors. We use these data to provide valuable information on the use of different optical
sensors toTo monitor the questions,
answer these phenological change the
we recorded of greenness
High Arcticof sixvegetation
High Arcticand present
plant data on the
species/groups
across an entire
effectiveness growingvegetation
of different season using data collected
indices from ordinary
in adequately digital cameras
determining plant and two different
phenology in a low
NDVI sensors. We
productivity environment. use these data to provide valuable information on the use of different optical
sensors to monitor the phenological change of High Arctic vegetation and present data on the
effectiveness
2. Materials and of different vegetation indices in adequately determining plant phenology in a low
Methods
productivity environment.
2.1. Study Area and
2. Materials Equipment
and Methods Set-Up
The study was conducted in Adventdalen, central Svalbard, Norway (78°10′N, 16°02′E; Figure 1a,b).
2.1. Study Area and Equipment Set-Up
Adventdalen is one of the main valley systems in High Arctic Svalbard, with typically open tundra
dominated Thebystudy
ridge,was conducted
heath and marshin Adventdalen,
vegetation. The central
studySvalbard,
area was Norway
situated(78◦on
100the
N, 16 ◦ 020 E;
valley floor
Figure 1a,b). Adventdalen is one of the main valley systems in High Arctic Svalbard, with typically
between elevations of approximately 25–100 masl. Six locations were selected for sensor placement
open tundra dominated by ridge, heath and marsh vegetation. The study area was situated on
in order to record measures of plant greenness in different vegetation types. The vegetation types selected
the valley floor between elevations of approximately 25–100 masl. Six locations were selected
covered the dominating plant species of the area, such as: Cassiope tetragona; Dryas octopetala/Salix polaris;
for sensor placement in order to record measures of plant greenness in different vegetation types.
C. tetragona/D.
The vegetationoctopetala. Likewise,
types selected graminoid/Salix
covered polaris;
the dominating graminoid/bryophyte
plant and the
species of the area, such Luzula spp.
as: Cassiope
vegetation types
tetragona; were
Dryas included. The
octopetala/Salix ‘graminoid’
polaris; type contained
C. tetragona/D. a mixturegraminoid/Salix
octopetala. Likewise, of grasslike plant species,
polaris;
the majority of which were
graminoid/bryophyte andgrasses. Ourspp.
the Luzula study was therefore
vegetation representative
types were of the
included. The vegetation
‘graminoid’ typefound
across lower aelevations
contained mixture ofin Svalbard.
grasslike plantThese
species,types cover up
the majority to 10.2%
of which were(for the Dryas
grasses. Our studyand was
Cassiope
therefore representative
communities), of the vegetation
3.4% (graminoid/Salix found
polaris), and across
2.7% lower elevations in Svalbard.
(graminoid/bryophytes) These
of the land types
cover based
cover up to 10.2% (for the Dryas and Cassiope communities), 3.4% (graminoid/Salix
on the vegetation map for Svalbard [33]. Such High Arctic vegetation is characterised by having a polaris), and 2.7%
very(graminoid/bryophytes)
short growing season,oflow the biomass
land coverproductivity
based on the and vegetation
plant map for Svalbard
heights of c. 5–10[33].
cmSuch
[34].High
At each
Arctic vegetation is characterised by having a very short growing season, low biomass productivity
location, sturdy metal support apparatus were driven into the soil substrate and secured with three
and plant heights of c. 5–10 cm [34]. At each location, sturdy metal support apparatus were driven
metal guy ropes (Figure 1c). All sensors were securely attached to the support apparatus at a height
into the soil substrate and secured with three metal guy ropes (Figure 1c). All sensors were securely
of 2 m above ground level (Figure 1c,d). The design of the supporting apparatus minimised lateral
attached to the support apparatus at a height of 2 m above ground level (Figure 1c,d). The design of
movement due to wind
the supporting and minimised
apparatus ensured measurements
lateral movement fromduethe
to sensors
wind andwere recorded
ensured consistently
measurements from over
the same fixed area throughout the season.
the sensors were recorded consistently over the same fixed area throughout the season.

Figure 1. Cont.
Remote Sens. 2016, 8, 847 4 of 17

Figure 1. Maps of (a) location of the study area in Svalbard; (b) sensor locations in Adventdalen, Central
Svalbard; (c) and (d) images of the Decagon Normalized Difference Vegetation Index (NDVI) surface
reflectance sensor, hemispherical sensor and red-green-blue wavelength (RGB) camera. The black
symbol in (a) shows the location of the study site in Svalbard and in (b) the locations of the six
monitoring sites in Adventdalen. Rivers are indicated in blue in (a,b) and contour lines with elevations
(masl) are also displayed in (b).

2.2. Sensor Descriptions and Monitoring Setup

Plant greenness was captured via two different near remote sensing techniques: NDVI, measured
with sensors sensitive to red and near infra-red wavelengths; and greenness indices derived from
images taken with standard digital red-green-blue wavelength (RGB) cameras. NDVI was recorded
with two different devices; active and passive sensors. NDVI was measured at three of the fixed
stations with in-situ Decagon Spectral Reflectance Sensors SRS-Nr [35] (hereafter Decagon sensor,
which are now under test by several research teams, e.g., [36]) attached to programmable data loggers
(Decagon Em50), which allowed full control of sensor activity. The Decagon sensors are passive sensor
instruments and measure radiation in the near infrared (NIR: 810 ± 10 nm) and red (650 ± 10 nm)
bandwidths. Each Decagon sensor was installed off-nadir (at 18◦ ), thereby recording NDVI values over
a spot diameter of 1.3 m. One upwards pointing Decagon hemispherical sensor SRS-Ni was installed
and the incident radiation data collected was used to calibrate all the Decagon sensors. Data were
recorded at four hourly intervals, beginning at midnight, for both NDVI and hemispherical reflectance
sensor. Both NDVI and calibration values were taken as an average of six readings through the day.
Sensors were installed on 4 June 2015 and retrieved on 31 August 2015, thereby resulting in data that
covered 89 days of the growing season. NDVI was also measured directly at each plot with a Trimble
Greenseeker Handheld Crop Sensor [37] (hereafter, Greenseeker). The Greenseeker is a portable, active
sensor device that requires manual input for operation: a trigger is pulled which turns the sensor on,
whereby light emitting diodes then beam near infrared (NIR: 780 ± 10 nm) and red (670 ± 10 nm)
radiation onto the plant canopy, with the amount of light reflected back to the device then measured
via silicon diodes. The device has no capacity for data logging, and it was not possible to take all
measurements at the structured time intervals that coincided exactly with data recorded by the other
sensors. However, since the Greenseeker is an active sensor that both emits and measures light, it is
not limited by constraints such as cloud cover, atmospheric pollution, shadows and humidity that
accompany passive systems [38] such as the Decagon sensors. Thus, although data from the Decagon
sensors and Greenseeker device were recorded at different times of the day, NDVI values from the
same location should be comparable. Operators were instructed to use the device for nadir sampling
(thereby minimising any error associated with angle of view), at a height above ground level of 0.9 m
(manufacturer instructions indicate use at 0.6–1.2 m) and thus measurements covered a spot diameter
of 0.38 m. The Greenseeker was used to record NDVI values at each of the six monitoring locations at
a minimum of twice weekly intervals between 18 June and 28 August 2015, giving 31, 33 or 34 days of
data (dependent on location).
Remote Sens. 2016, 8, 847 5 of 17

To enable greenness indices to be calculated for different plant species/groups throughout

the growing season, images were captured with digital RGB cameras installed at each of the six
monitoring locations. Five Brinno GardenWatch cameras [39] and a Cuddeback camera [40] were used.
The GardenWatch camera has a resolution of 1.3 megapixels and recorded images every four hours,
beginning at midnight from 6 June to 31 August, giving 87 days of data. The Cuddeback camera has a
resolution of 20 megapixels and recorded one image every hour from 18 June to 31 August, giving
75 days of data. Each RGB camera was attached in the nadir position to the metal support apparatus
described above (Figure 1d). The RGB cameras captured images over the same area that NDVI was
recorded by Decagon sensors and the Greenseeker device and covered an area of 1.4 m × 1.1 m.

3. Data Preparation
Data from the Decagon sensors were calibrated using information on incident red and near
infrared radiation collected by the hemispherical Decagon sensor. These data were used to calculate a
calibration constant α:
α = Ir/In (1)

where Ir is the incident red radiation and In the incident near-infrared radiation. Calibration of the
values recorded by the Decagon sensors was then possible using the formula:

αRn − Rr
NDVI = (2)
αRn + Rr

where Rn is the reflected near infrared radiation and Rr the reflected red radiation.
Vegetation indices (greenness indices) were calculated using information from the red, green and
blue bands of the RGB images captured by the digital cameras throughout the growing season. Among
six images taken every day, preferentially the mid-day images (time 12:00) were chosen. If fog, rain or
other environmental conditions deteriorated image quality, the very best picture of that particular day
was chosen. To ensure equivalent areas of vegetation at each location were compared throughout the
growing season, masks were applied to specific defined areas of interest (AOI) in each of the images.
Polygons were drawn around AOI, and converted to raster with the same extent and resolution as the
images. From the areas within each mask, average digital numbers (DNs) were calculated for each
vegetation type. For each RGB image, DN information was collected from the red, green and blue
bands and was used to calculate three different greenness indices (2G_RBi [22], Channel G% [22,32]
and Green-Red Vegetation Index (GRVI) [28,41]), as follows:

2G_ RBi = 2GDN − ( R DN + BDN ) (3)

Channel G% = GDN /Total RGBDN (4)

GRVI = ( GDN − R DN ) / ( GDN + R DN ) (5)

where GDN , RDN and BDN represent the digital numbers for the green, red and blue
channels respectively.

4. Statistical Analyses
All statistical analyses were carried out in R (version 3.1.1). Firstly, to assess the ability of
three different greenness indices (GRVI; 2G_RBi, and; channel G%) derived from RGB image data
to capture the same patterns of change in plant greenness observed with NDVI values, we used
Pearson’s correlations to compare values from those three greenness indices with NDVI values
recorded by Decagon sensors and the Greenseeker device. Secondly, to determine how well the
NDVI devices and the best RGB greenness index captured the changing patterns of plant greenness
during the entire growing season, we used linear models with a second order polynomial function to
determine the significance of relationships between day of year (DOY) and (i) Decagon-derived NDVI;
Remote Sens. 2016, 8, 847 6 of 17

(ii) Greenseeker-derived NDVI; and (iii) RGB greenness index. Typically, the NDVI values within a
vegetation type or measuring NDVI of individual plant species, follows a unimodal or parabolic curve
throughout a growing season [16]. The second order polynomial function is among the best-suited
method to describe such pattern. Due to high day-to-day variability in GRVI values, these data were
filtered. GRVI values greater than one standard deviation from the mean have been omitted from
the analyses to exclude obviously erroneous data. Finally, we used Pearson’s correlations to compare
NDVI values recorded by Decagon sensors and the Greenseeker device in three different vegetation
types (graminoid/S. polaris; C. tetragona; and C. tetragona/D. octopetala vegetation). Where significant
correlations were evident, we then used linear models to determine the relationships between the
NDVI values recorded by the two different sensors.

5. Results

5.1. Comparison of Different RGB Greenness Indices

We assessed the ability of three different greenness indices (GRVI, 2G_RBi and channel G%)
derived from RGB images to record changes in plant greenness during the growing season by
comparison with NDVI values obtained from the Decagon and Greenseeker devices. The GRVI
had significant correlations with the NDVI values recorded in all vegetation types, with the exception
of Luzula spp., where the sample size was small due to RGB equipment failure during the early part of
the growing season (Table 1). The 2G_RBi and channel G% indices were much less well matched with
NDVI, with significant correlations only occurring for those vegetation types containing C. tetragona
(Table 1).

Table 1. Pearson’s correlations between NDVI and three different RGB greenness indices in six different
High Arctic vegetation types. The NDVI measurement instruments used were Decagon sensors (D) and
a Greenseeker device (G). Greenness index values greater than one standard deviation from the mean
have been omitted from the analyses to exclude obviously erroneous data. t = t-statistic tn = the valid
sample numbers after filtering the time serial data. Statistically significant relationships are highlighted
in bold.

NDVI GRVI 2G_RBi Channel G%

Vegetation
Sensor t p r t p r t p r
D t64 = 9.74 <0.001 0.77 t72 = 1.34 0.19 0.16 t68 = 2.00 0.05 0.24
Graminoid/Salix polaris
G t24 = 2.39 0.03 0.44 t27 = 1.77 0.09 0.32 t24 = 1.21 0.24 0.24
D t45 = 6.08 <0.001 0.67 t65 = 2.90 0.005 0.34 t65 = 2.99 0.004 0.35
Cassiope tetragona
G t16 = 3.51 0.003 0.66 t23 = 2.31 0.03 0.43 t22 = 2.11 0.05 0.41
Luzula spp. G t11 = 1.97 0.075 0.51 t13 = 1.08 0.30 0.29 t11 = 0.44 0.67 0.13
Dryas octopetala/S. polaris G t16 = 4.90 <0.001 0.77 t15 < 0.001 0.99 <0.001 t15 = 1.72 0.12 0.41
D t51 = 5.77 <0.001 0.63 t69 = 4.12 <0.001 0.44 t68 = 4.00 <0.001 0.44
C. tetragona/D. octopetala
G t25 = 0.91 0.37 0.18 t29 = 1.35 0.19 0.24 t30 = 1.97 0.06 0.34
Graminoid/bryophyte G t22 = 5.67 <0.001 0.77 t17 = 1.48 0.16 0.34 t16 = 0.69 0.50 0.17

5.2. Capturing Changes in Plant Greenness during the Growing Season

The general pattern of change in plant greenness as the season progressed, recorded by NDVI
sensors and the GRVI was similar in all vegetation types: values increased from the start of data
recording, immediately after snow melted on 4 June (DOY 155), reached a maximum between 17 July
(DOY 198) and 29 July (DOY 210), then after a period of peak growth the values decreased until
the end of data recording on 30 August (DOY 242) when the first snowfall of autumn occurred
(Figure 2). Hence, the start of the growing season (greening-up period) occurred from c. 4–19 June
(DOY 155-170), the period of plant growth from c. 20 June–29 July (DOY 171-210) and senescence
from c. 30 July (DOY 211) onwards (Figure 3). The evergreen shrub C. tetragona, however, seemed to
have a slightly earlier start of the growing season, around 3 June (DOY 153-155), followed by the other
Remote Sens. 2016, 8, 847 7 of 17

species/species groups. The pattern during mid-season differed between some plant species/groups:
e.g., where graminoids (mostly grasses) were present, both NDVI and GRVI values reached a sharp
peak mid-season (DOY 195-200) and then dropped off fairly rapidly (Figure 2a,f). By contrast, the
other plant species/groups (including Luzula) appeared to have a more prolonged period during
mid-season when higher NDVI and GRVI values were maintained (Figure 2b–e). Towards the end of
the season (from 18 August or DOY 230 onwards), relatively large daily variations in NDVI and GRVI
values were evident in graminoid/S. polaris (Figure 2a); C. tetragona (Figure 2b); and C. tetragona/D.
octopetala (Figure 2e) vegetation. In fact, at the end of August, on some occasions greenness index
values equalled or exceeded values recorded during peak season, with this pattern most evident in
the Decagon measurements, but also observed in the GRVI. The relationships between DOY and the
plant greenness measure (NDVI or GRVI) were significant for all vegetation types, with the exception
of GRVI values for the Luzula spp. (Table 2) where the sample size was small due to RGB equipment
failure early in the season.

Table 2. Relationships between day of year and values of different vegetation indices in six different
High Arctic vegetation types. GRVI values greater than one standard deviation from the mean have
been omitted from the analyses to exclude obviously erroneous data.

Decagon NDVI Greenseeker NDVI GRVI

Vegetation
F p R2 F p R2 F p R2
Graminoid/Salix polaris F2,84 = 386 <0.001 0.90 F2,30 = 8.34 0.001 0.32 F2,64 = 30.5 <0.001 0.47
Cassiope tetragona F2,84 = 146 <0.001 0.77 F2,30 = 17.7 <0.001 0.51 F2,44 = 68.4 <0.001 0.75
Luzula spp. - - - F2,31 = 21.5 <0.001 0.55 F1,27 = 0.02 0.89 0.04
Dryas octopetala/S. polaris - - - F2,31 = 20.4 <0.001 0.54 F2,45 = 25.7 <0.001 0.51
C. tetragona/D. octopetala F2,84 = 415 <0.001 0.91 F2,31 = 9.14 <0.001 0.33 F2,51 = 62.4 <0.001 0.70
Graminoid/bryophyte - - - F2,28 = 22.3 <0.001 0.59 F2,56 = 83.7 <0.001 0.74

5.3. Comparison of Different NDVI Sensors

NDVI values recorded by the Decagon sensors and the Greenseeker device were well correlated
in graminoid/S. polaris (t31 = 7.47, p < 0.001, r = 0.80), C. tetragona (t31 = 6.88, p < 0.001, r = 0.78) and
C. tetragona/D. octopetala vegetation (t32 = 5.55, p < 0.001, r = 0.70). Highly significant (p < 0.001)
positive trends were evident in the relationships between NDVI recorded by the Decagon sensors
and the Greenseeker device, in graminoid/S. polaris (Figure 4a), C. tetragona (Figure 4b) and
C. tetragona/D. octopetala vegetation (Figure 4c). Looking across the entire growing season, it was
evident that both NDVI devices (Decagon and Greenseeker) captured the changes in plant greenness
throughout the growing season (Figure 2). However, NDVI values recorded by the Greenseeker device
were consistently lower than those from the Decagon sensors (Figure 2a,b,e and Figure 4). Although
the relationships between NDVI recorded by Decagon sensors and the Greenseeker device were very
similar for graminoid/S. polaris (Figure 4a) and C. tetragona vegetation (Figure 4b), it did differ rather
more for C. tetragona/D. octopetala vegetation (Figure 4c).
Remote Sens. 2016, 8, 847 8 of 17
Remote Sens. 2016, 8, 847 7 of 16

Figure 2. NDVI and greenness index values from six different High Arctic plant communities
Figure 2. NDVI and greenness index values from six different High Arctic plant communities
throughout the growing season. Readings were taken between 5 June (day of year = 156) and
throughout the growing season. Readings were taken between 5 June (day of year = 156) and
30 August (day of year = 242) 2015 in: (a) Graminoid/Salix polaris; (b) Cassiope tetragona; (c) Luzula spp.;
30 August (day of year = 242) 2015 in: (a) Graminoid/Salix polaris; (b) Cassiope tetragona; (c) Luzula spp.;
(d) Dryas octopetala/Salix polaris; (e) Cassiope tetragona/Dryas octopetala; and (f) Graminoid/bryophyte
(d) Dryas octopetala/Salix polaris; (e) Cassiope tetragona/Dryas octopetala; and (f) Graminoid/bryophyte
vegetation. NDVI was recorded using Decagon surface reflectance sensors (black circles) and a
vegetation. NDVI was recorded using Decagon surface reflectance sensors (black circles) and a
Trimble Greenseeker handheld sensor (open circles); the Green-Red Vegetation Index (GRVI) values
Trimble Greenseeker handheld sensor (open circles); the Green-Red Vegetation Index (GRVI) values
(grey squares) were calculated from red and green channel data from RGB images.
(grey squares) were calculated from red and green channel data from RGB images.
Remote Sens. 2016, 8, 847
Remote Sens. 2016, 8, 847
9 of 17
8 of 16

Figure
Figure 3. 3.RGB
RGB camera
camera images
images ofofsix
sixHigh
HighArctic plant
Arctic species/groups
plant from from
species/groups Svalbard during during
Svalbard plant
green-up (10 June DOY 160), peak plant growth (19 July DOY 200) and senescence
plant green-up (10 June DOY 161), peak plant growth (19 July DOY 200) and senescence(28 August DOY 240).
(28 August DOY 240).
NDVI devices (Decagon and Greenseeker) captured the changes in plant greenness throughout the
growing season (Figure 2). However, NDVI values recorded by the Greenseeker device were
consistently lower than those from the Decagon sensors (Figures 2a,b,e and 4). Although the
relationships between NDVI recorded by Decagon sensors and the Greenseeker device were very
similar for graminoid/S. polaris (Figure 4a) and C. tetragona vegetation (Figure 4b), it did differ rather
Remote Sens. 2016, 8, 847 10 of 17
more for C. tetragona/D. octopetala vegetation (Figure 4c).

0.60
a. Graminoid S al i x po l ar i s
y = 3.61(x) - 2.26
0.55

NDVI (Greenseeker)
0.50

0.45

0.40

0.35

0.30
0.40 0.45 0.50 0.55 0.60

NDVI (Decagon)
0.65
b. C assi ope t et ragon a

y = 3.60(x) - 2.11
0.60
NDVI (Greenseeker)

0.55

0.50

0.45

0.40

Remote Sens. 2016, 8, 847 10 of 16

0.35
0.45 0.50 0.55 0.60 0.65
0.60
c. C assi ope t et ragon a Dr yas oct opet al a

y = 2.94(x) - 1.83
0.55
NDVI (Greenseeker)

0.50

0.45

0.40

0.35

0.30
0.40 0.45 0.50 0.55 0.60

Figure 4.
Figure 4. Comparison
ComparisonofofDecagon
Decagonsurface
surfacereflectance sensor-derived
reflectance sensor-derived NDVI
NDVIand(passive)
Trimble Greenseeker-
and Trimble
derived NDVI (active)
Greenseeker-derived from(active)
NDVI different vegetation
from differenttypes in High
vegetation Arctic
types Svalbard.
in High ArcticReadings
Svalbard.were taken
Readings
between
were taken 18 June (day18
between of June
year =(day
169) of
and 28 August
year = 169) (day
and of
28 year = 240)
August 2015
(day ofin: (a) Graminoid/Salix
year = 240) 2015 in:
polaris;
(a) (b) Cassiope tetragona,
Graminoid/Salix polaris; (b)and; (c) Cassiope
Cassiope tetragona/Dryas
tetragona, octopetala
and; (c) Cassiope vegetation.
tetragona/Dryas Fittedvegetation.
octopetala lines from
Fitted lines from the linear models are shown. The closer points are to the dashed line (y = x), theare
the linear models are shown. The closer points are to the dashed line (y = x), the more similar the
more
values are
similar recorded by the
the values Decagon
recorded bysensors and the
the Decagon Greenseeker
sensors and thedevice.
Greenseeker device.

6. Discussion
6. Discussion
Thereare
There aremany
manyopportunities
opportunitiesforforusing
usingnear
nearremote
remote sensing
sensing to to capture
capture environmental
environmental change
change in
in the remote Arctic. Indeed, digital cameras have been used to monitor such dynamic
the remote Arctic. Indeed, digital cameras have been used to monitor such dynamic processes as snow processes as
snow cover and melt [42–44], glacier flow [45] and animal movements [46]. Here, we demonstrate
cover and melt [42–44], glacier flow [45] and animal movements [46]. Here, we demonstrate the ability the
ability
of of inexpensive
inexpensive digitaland
digital cameras cameras and NDVI
field-based field-based NDVI
devices devices
to monitor theto monitor dynamics
vegetation the vegetation
of six
dynamics of six common and widespread plant species/groups in the High Arctic.
common and widespread plant species/groups in the High Arctic. Digital cameras captured data of Digital cameras
captured data of sufficient quality throughout the growing season to enable the calculation of
vegetation indices for each plant species/group. Of the three passive RGB derived greenness indices
assessed, one was highly correlated with NDVI values in all plant groups studied. Thus, digital
cameras can be successfully used for plant phenological monitoring at high latitudes.
In contrast to other studies that have compared the RGB derived vegetation indices 2G_RBi and
Remote Sens. 2016, 8, 847 11 of 17

sufficient quality throughout the growing season to enable the calculation of vegetation indices for each
plant species/group. Of the three passive RGB derived greenness indices assessed, one was highly
correlated with NDVI values in all plant groups studied. Thus, digital cameras can be successfully
used for plant phenological monitoring at high latitudes.
In contrast to other studies that have compared the RGB derived vegetation indices 2G_RBi and
channel G% with NDVI and found strong correlations [29,32] or similarity in the seasonal patterns
observed [22,47], we found these relationships to be lacking for all the common High Arctic plant
species/groups monitored, except for plots where C. tetragona was present. Yet even when this plant
species was present, although the correlations of 2G_RBi and channel G% with NDVI were significant,
the r values were low (<0.45). This may be due to differences in the types of vegetation surveyed, since
most of the previous studies using the 2G_RBi and channel G% vegetation indices have described the
phenology of broadleaf forest canopies, low-latitude grasslands and agricultural crops [22,29,32,47].
Indeed, even the heath, fen and copse vegetation monitored by Westergaard-Nielsen et al. [32] in
Greenland with digital cameras, where they found channel G% and 2G_RBi indices to be significantly
correlated with NDVI, was situated in the Low Arctic, where the vegetation structure and species
composition is quite different to that found at higher latitudes. Although a study from northern
Svalbard (79◦ 400 N) using imagery from the WorldView-2 satellite and an airborne RGB camera
found channel G% values to be reasonably well correlated with NDVI, the vegetation surveyed
(creeping saltmarsh grass (Puccinellia phryganodes) and moss-crust tundra communities) [48] was very
different to that presented in this study. Furthermore, channel G% and 2G_RBi experience greater
diurnal variations in values as they include data from the blue channel, which is strongly affected by
changes in solar irradiance such as cloudy conditions [49]. Cloud cover is common in Svalbard [50],
therefore our season-long study may have been unable to generate stable channel G% and 2G_RBi
values due to noise in the blue channel related to atmospheric conditions. These diurnal variations
were not apparent in the derivation of channel G% values for vegetation in northern Svalbard as that
study used data from only one day [48]. Additionally, the spatial scale of operation may have had an
effect, i.e. the cameras used in our study monitored vegetation over an area of c. 1 m2 , whereas previous
studies monitored vegetation over the scale of a few tens to several hundreds of square metres.
We did, however, have more success with the RGB derived GRVI (passive), which was significantly
and strongly correlated with NDVI values despite fluctuations in the RGB camera derived index. Such
variations may be due to diurnal differences in illumination, since the white balance and exposure
settings of the RGB cameras we used were fixed to automatic with no option available to change
these settings. Therefore, if the equipment allows, we recommend changing the white balance from
automatic to a fixed setting as this can stabilise diurnal fluctuations in the indices calculated [51].
Nevertheless, our results support the findings of Motohka et al. [28] and von Bueren et al. [52] who
found that the GRVI could be used to successfully monitor phenological change in vegetation. We have,
therefore, extended the applicability of use of the GRVI to detect phenological change from low-latitude
deciduous broadleaf and coniferous forest, grassland and rice paddy vegetation to include High Arctic
vegetation. Motohka et al. [28] used the transition from negative to positive GRVI values to detect
phenological change as they found negative values to equate with soils and positive values with green
vegetation. However, we were unable to replicate this with High Arctic vegetation. Most of the GRVI
values calculated in our study were negative, a likely reflection of the sparse cover of High Arctic
plants [34] and the presence of black cryptogamic crust, which is widespread in the High Arctic [53],
in almost all of our monitoring plots. Thus, given these limitations, the use of an absolute threshold
GRVI value to define transitions between phenological stages in High Arctic vegetation may only be
possible via monitoring at the individual species level rather than across mixed plant assemblages.
In addition, if the main reason that the GRVI index performed better was the lack of blue band, would
the values be just as good with a simple vegetation difference? Studies examining a variety of plants
and stress factors in agricultural landscapes have found simple ratio indices to be most strongly
affected by plant stress as well as phenological development [54,55], and this might also be the case for
Remote Sens. 2016, 8, 847 12 of 17

natural plants in Arctic environments. Nevertheless, the GRVI index clearly tracked the changes in
plant greenness throughout the season and, hence, can be used effectively to monitor phenological
change of High Arctic vegetation. We therefore recommend that future studies, making use of an RGB
derived greenness index to monitor vegetation phenological change, assess more than one index in
order to find the most representative for the plant species being studied.
As the growing season progressed, both NDVI measures (active and passive) and the passive
RGB derived GRVI tracked similar patterns of changes in growth for all plant species monitored:
values increased after snowmelt, reached a peak at mid-season before declining. However, as reported
from field observational studies [11,56,57], there were noticeable differences in these patterns between
species/groups. For instance, vegetation plots containing graminoids reached a well-defined and short
peak in index values before declining sharply, whereas plots containing C. tetragona and D. octopetala
had broader mid-season peak values as well as increased values at the end of the growing season/study
period. For C. tetragona and D. octopetala this pattern may have been be due to recovery after set-back
or injury to these species caused by harsh winter conditions. Indeed, large patches of dead C. tetragona
vegetation were observed across Svalbard that summer (pers. obs.), presumably due to frost damage
caused by lack of sufficient winter snow cover [58], possibly due to periods of snow thaw followed
by re-freeze in the winter [59]. This species appears particularly susceptible to frost damage as the
flower and leaf buds are erect, hence occurring at a greater height above ground (5–15 cm) than other
High Arctic plant species that are characterised by having a prostrate structure [59]. The second
peak in greenness values observed late in the season could also be partly attributed to the elongated
growing season exhibited by bryophytes that lack senescence, as has been observed in Greenland [60].
This factor, however, depends on the amount of bryophytes present (in the study plot) that may take
advantage of increased precipitation during the end of growing season in 2015, and this increased
wetness may also contribute to sustained growth for stands of evergreen Cassiope tetragona that not had
entered senescence. However, data from the graminoid/bryophyte community (Figure 2f), in which
the bryophytes contributed significantly more to the signal than the other communities in this analysis,
showed a rapid decrease from mid-season (DOY 200) towards the end of the season, indicating that
the bryophyte activity may not explain the end season peak in the dwarf shrub (C. tetragona and
D. octopetala) dominated plots. A late season peak is also shown in Graminoid/Salix polaris vegetation
plot (Figure 2a). Both graminoids and Salix are deciduous, normally changing colour and losing leaves
around DOY 230 [11] so extended late-season growth for these plants may be an unlikely explaination
for the second peak observed in Figure 2a.
The second peak (DOY 225-240) is very marked in the Decagon NDVI data and to a lesser degree
in the GRVI data, but not in the Greenseeker NDVI data. Other measurements by our research group
recorded an increase in soil moisture in this same period. Whether our data really shows late season
growth or, rather, differential instrumental response to increased moisture in late season, is impossible
to determine with our present data set but is indeed an area for further research.
The increased variation in vegetation index values observed towards the end of the season
was likely due to senescence producing changes in leaf colouration, a process that occurs
over a more prolonged period than green-up, and also has species-specific timing [11,57,61].
Although Richardson et al. [22] found that RGB derived indices increased more slowly than NDVI
values, we did not find this to be the case with High Arctic vegetation, thus suggesting that both NDVI
and the GRVI used in this study captured the same vegetation attributes.
The greater variability in NDVI values obtained by the Greenseeker device compared with the
Decagon sensors may be due to the Decagon sensors recording information at fixed times (midday),
whereas the times at which the Greenseeker device recorded data were variable (but occurred between
the hours of 10:00 and 14:00). However, the variability in values was low and in a study of pine forest
in Finland, Wang et al. [62] found little daily variation in ground-based NDVI, particularly in the two
hours either side of midday. Daily variations in NDVI may also have been caused by differences in
weather conditions (sunny, partly cloudy and full cloud cover) as dense clouds are known to alter the
Remote Sens. 2016, 8, 847 13 of 17

quality of incident and reflected radiation [62]. Svalbard, however, has an oceanic climate with much
cloud cover and few days with clear skies [50,63]. Consequently, during the growing season most
days experienced cloud cover and we found little variation in NDVI values that could be attributed
to weather conditions. Additionally, some differences in absolute NDVI values may be expected
between the two sensor types because they operate at slightly different bandwidths [64]. However,
the consistently lower values obtained from the active Greenseeker sensor compared to the passive
Decagon sensors, also reported by Fitzgerald [65] and Yao et al. [66], can most likely be attributed to
the different modes of operation that the two sensor types employ: the Greenseeker device is an active
sensor, generating its own radiation for NDVI measurements, whereas the Decagon sensors are passive
instruments, using reflected and incident radiation which has been calibrated to a constant using a
hemispherical sensor [36]. For active sensors such as the Greenseeker, the advantage of not requiring
calibration is nonetheless counterbalanced by the restricted bandwidth of radiation available for use
as a light source. This limits their use to proximal sensing only [66] and reduces their performance
when compared with that of passive sensors such as the Decagon devices [65]. However, as stated by
Fitzgerald [65] and noted in this study, such differences in performance between active and passive
sensors in measuring greenness are small. Therefore, as the efforts to inter-calibrate NDVI values
derived from different satellite-based sensors show [67], it is evident that the same function could
be performed with near remote sensing NDVI sensors, although not with the same accuracies as for
the satellite-based sensors. A study by Yao et al. [66] comparing ASD Field Spec Pro spectrometer,
CropScan MSR 16 and GreenSeeker RT 100 indicated that the vegetation indices from different sensors
could be inter-calibrated. Their inter-calibration model showed that nearly equivalent NDVIs between
these sensors could be achieved. Although there appears to be an absence of a universal equation
representative of all High Arctic plant species that could be used to convert values obtained from
different NDVI devices, species-specific inter-calibrations would certainly be possible. Combining the
use of both types of devices could be helpful for extending the monitoring of phenological change in
different plant species, thus enable spatial upscaling towards landscape level and above.

7. Conclusions
The near remote sensing devices Decagon and RGB digital camera (both passive) and Greenseeker
(active), seem to offer great opportunities for monitoring phenological change in High Arctic vegetation:

1 Comparing the Decagon and Greenseeker NDVI correlation for the three vegetation types
equipped with Decagon sensors, the r was 0.80, 0.78 and 0.70 respectively.
2 However, the (passive) Decagon sensor had higher correlations with the GRVI than the (active)
Greenseeker (Decagon 0.77, 0.67 and 0.63, Greenseeker 0.44, 0.66 and 0.18).
3 Among the three RGB greenness indices derived from the digital cameras, the GRVI had the
highest and most significant correlation of NDVI with both (passive) Decagon and (active)
Greenseeker derived NDVI. For the 2G_RBi and Channel G%, only two vegetation types had
significant correlations with Decagon (r = 0.34–0.44) and the Greenseeker NDVI (r = 0.43).
4 The greater variability in NDVI measurement and poorer performance of (active) Greenseeker
compared to (passive) Decagon indicate the need for more precise and rigid procedures for field
measurement; the Greeenseeker should be placed in a fixed position, aspect, slope and elevation
for each field point measured.
5 Correlations between NDVI values derived from (passive) Decagon/(active) Greenseeker and the
RGB derived vegetation indices obtained from the digital cameras, especially the GRVI, indicate
that both approaches capture similar vegetation attributes and are capable of being used to
monitor phenological change in different plant species/groups. Thus, both NDVI sensors and
RGB cameras could be used to establish an High Arctic near remote sensing monitoring network
with the aim of validating high spatial resolution satellite based products.
Remote Sens. 2016, 8, 847 14 of 17

6 Inexpensive RGB cameras offer a more affordable alternative to the more specialized and expensive
NDVI sensors for monitoring plant greenness. This may enable a greater spatial coverage for
field campaigns.

Acknowledgments: We thank Mark Gillespie, Nanna Baggesen, and Anne Marit Vik for field assistance.
The University in Svalbard (UNIS) provided logistical support. This work was funded by the Norwegian Research
Council through the ‘SnoEco’ project (project No. 230970) and Arctic Field Grant (No. 246110/E10). It was
supported by the ESA Prodex project ‘Sentinel-2 for High North Vegetation Phenology’ (contract No. 4000110654),
the EC FP7 collaborative project ‘Sentinels Synergy Framework’ (SenSyF), funding from The Fram Centre
Terrestrial Flagship, also from the EEA Norway Grants (WICLAP project, ID 198571), and from the GRENE
Arctic Climate Change Research Project, Ministry of Education, Culture, Sports, Science and Technology in Japan.
Author Contributions: All authors contributed to the study design, data preparation and/or interpretation and
paper writing. In addition, Lennart Nilsen and Hans Tømmervik set up the field equipment, Helen B. Anderson
and Stein Rune Karlsen analysed data, Helen B. Anderson led the writing. Elisabeth J. Cooper obtained funding
and is project leader for the SnoEco project, of which this study is a part.
Conflicts of Interest: The authors declare no conflict of interest.

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