Philippa Kaur

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An experiment in secondary forests in the Democratic Republic of the Congo finds that calcium, an overlooked soil nutrient, is scarcer than phosphorus, and represents a potentially greater limitation on tropical forest growth.Ecology can reveal distributional patterns and dynamics in nature. One approach used is studying the elemental composition of plants, which has been linked to ecological processes such as growth, diversity or water use efficiency. More recently, elemental composition has been detected as a cofactor in governing the carbon sink capacity of plants, and therefore climate change mitigation1,2,3. This discovery has added an extra layer of urgency to the field, which now aims to better understand and predict global change. The study of nitrogen and/or phosphorus has until now received most of the attention of plant ecologists: nitrogen is the most abundant element in dry leaves after hydrogen and carbon, forms the main structure of proteins and is strongly linked to photosynthesis4. Phosphorus represents around one-tenth of nitrogen abundance in leaves and is key in energy storage and nucleic acids. However, although these represent only two of the many chemical elements that are in flux throughout ecosystems, whether others may have a dominant role in ecosystem dynamics is an open question. Writing in Nature Ecology & Evolution, Bauters et al.5 share some evidence to motivate broadening out from the dominant focus on nitrogen and phosphorus in terrestrial ecology, by revealing a crucial limiting role of calcium in the dynamics of tropical forest succession. More

Sample collection and hydrographySampling was conducted aboard the University of Victoria’s MSV John Strickland either weekly, biweekly or monthly between 11 March 2010 and 15 November 2017 in Saanich Inlet at 48.59°N, 123.50°W (Fig. 1). To standardize measurements and due to biological significance, seawater was collected from the euphotic zone. Sampling depths corresponded to approximately 100, 50, 15, and 1% of the photosynthetically active radiation (PAR) at the surface (Io). These “light” depths were either determined using a CTD-mounted PAR sensor or a Secchi disk. CTD profiles were performed prior to each seawater cast to measure depth, temperature and conductivity of the water column, and PAR, fluorescence, and dissolved oxygen (when available).Seawater from each light depth was collected using Niskin or GO-FLO bottles on either a rosette sampler or an oceanographic wire. When possible, individual samples were collected directly from the Niskin or GO-FLO bottles. When time was not sufficient to allow direct sampling, bulk samples of seawater from each depth were collected into acid-washed polyethylene carboys, kept cold in the dark, and homogenized before sub-sampling for the individual measurements.Dissolved nutrientsFor the measurements of nitrite (NO2−), nitrate and nitrite (NO3− + NO2−), phosphate (PO43−) and Si(OH)4, seawater samples from each light depth were syringe-filtered through a combusted 0.7 µm (nominal porosity) glass fibre filter into acid-washed 30-mL polypropylene bottles and immediately frozen. All nutrient samples were stored at −20 °C until analysis. Concentrations of NO2−, NO3− + NO2−, PO43−, and Si(OH)4 were determined using an Astoria Nutrient Autoanalyzer (Astoria-Pacific, OR, USA) following the methodology of Barwell-Clarke and Whitney22. During 2014 and 2015, samples for the measurement of Si(OH)4 were collected separately from those for the other nutrients, filtered with a 0.6 µm polycarbonate membrane filter and stored at 4 °C. During this period, Si(OH)4 concentrations were determined manually using the molybdate blue colorimetric methodology23. Replicate (2 or 3) nutrient samples were taken at each depth; average data are presented in the published dataset and the figures (Fig. 2).Fig. 2Dissolved macronutrient concentrations in the euphotic zone of Saanich Inlet from March 11, 2010 to November 15, 2017. Left panels show depth-integrated concentrations (black bars on top) and time-series profiles (filled contour/scatter plots on bottom) for (A) nitrate plus nitrite (NO3− + NO2−), (B) phosphate (PO43−) and (C) silicic acid (Si(OH)4). In the time-series profiles, 2012–2013 data are not interpolated due to single-depth sampling. Grey shaded regions in top panels indicate the phytoplankton growing seasons considered for this study (March 1st – October 30th). Right panels show monthly-averaged depth profiles for the entire 8-year period, illustrating euphotic zone seasonality for each nutrient. The color scale bars on the far right apply to both the time-series vertical profiles and the 8-year seasonal plots. Sampling depths are indicated by round symbols. The year labels are positioned under the tick marks corresponding to January.Full size imageSuspended particulate matterTotal chlorophyll-aChlorophyll-a (Chl-a) was used as a proxy for phytoplankton biomass (Fig. 3A). For total Chl-a analysis, seawater samples (0.25–1 L) were gently vacuum filtered onto 0.7 µm (nominal porosity) glass fiber filters, which were then stored at −20 °C until analysis. Chl-a concentrations were determined using the acetone extraction and acidification method24,25. Acidification of samples decreased the likelihood of overestimation of Chl-a concentrations due to the presence of chlorophyll degradation products26. Filters were submerged in 10 mL of 90% acetone, sonicated for 10 minutes in an ice bath, and left to extract at −20 °C for 22 h. Following the extraction period, samples were allowed to equilibrate to room temperature (~2 h). Fluorescence of the acetone solution containing the extracted Chl-a was measured before and after acidification with 1.2 N hydrochloric acid using a Turner 10-AU fluorometer. The final concentrations of total Chl-a were calculated from measurements made before (Fo) and after (Fa) acidification using Eq. (1)25. The coefficient (τ) of Eq. (1), adapted from Strickland and Parsons25, was derived from a calibration of the Turner 10-AU fluorometer with known pure chlorophyll standards (Table 2).$${rm{C}}{rm{h}}{rm{l}} mbox{-} {rm{a}}(mu g,{L}^{-1})=frac{tau }{tau -1}ast ({rm{F}}{rm{o}}-{rm{F}}{rm{a}})ast 0.814ast left(frac{{rm{V}}{rm{o}}{rm{l}}.{rm{A}}{rm{c}}{rm{e}}{rm{t}}{rm{o}}{rm{n}}{rm{e}},{rm{e}}{rm{x}}{rm{t}}{rm{r}}{rm{a}}{rm{c}}{rm{t}}{rm{e}}{rm{d}}}{{rm{V}}{rm{o}}{rm{l}}.{rm{S}}{rm{e}}{rm{a}}{rm{w}}{rm{a}}{rm{t}}{rm{e}}{rm{r}},{rm{f}}{rm{i}}{rm{l}}{rm{t}}{rm{e}}{rm{r}}{rm{e}}{rm{d}}}right)$$
(1)
Fig. 3Biological particulate concentrations in the euphotic zone of Saanich Inlet from March 11, 2010 – November 15, 2017. Left panels show time-series profiles (filled contour/scatter plots) of (A) total chlorophyll-a (Total Chl-a), (B) particulate carbon (PC), (C) particulate nitrogen (PN), and (D) particulate biogenic silica (bSiO2). The 2012–2013 data are not interpolated due to single-depth sampling. In A, the bar plot in the top panel shows percent contribution of different size fractions to total Chl-a. In (B–D), black bars in top panels show depth-integrated concentrations. Grey shaded regions in bar plots indicate phytoplankton growing seasons considered for this study (March 1st – October 30th). Right panels show monthly-averaged depth profiles for the entire 8-year period, illustrating euphotic zone seasonality for each particulate. The color scale bars on the far right apply to both the time-series vertical profiles and the 8-year seasonal plots. Sampling depths are indicated by round symbols. The year labels are positioned under the tick marks corresponding to January.Full size imageSize fractionated chlorophyll-aTo determine the percent contributions of “pico” (0.7–2 µm), “small nano” (2–5 µm), “large nano” (5–20 µm) and “micro” ( >20 µm) phytoplankton to total Chl-a, seawater samples (0.25–1 L) separate from those used for total Chl-a) were consecutively filtered through 20, 5 and 2 µm polycarbonate membrane filters and 0.7 µm (nominal porosity) glass fiber filters. Between 2013 and 2017, the “pico” and “small nano” size classes were collected as one fraction (0.7–5 µm). Analysis of Chl-a concentrations for each size fraction followed the same procedure outlined for total Chl-a.Particulate carbon and nitrogenParticulate C and N measurements were obtained from seawater samples incubated for carbon (ρC) and nitrate uptake (ρNO3) rates (see section on “Uptake rates of carbon and nitrate” for methodology) (Fig. 3B,C). PC and PN measurements presented in this dataset were taken at the end of ρC and ρNO3 incubations; however, original (‘ambient’) values can be back calculated by subtracting the amount of C and N taken up during the incubation period from the final PC and PN values. The differences between after-incubation PC and PN data and back-calculated ambient values were not significantly different than the measurement error.Particulate biogenic silicaParticulate biogenic silica was used as a proxy for siliceous phytoplankton biomass (Fig. 3D). Seawater samples (0.5–1 L) from each depth were gently vacuum filtered through 0.6 µm polycarbonate membrane filters. Filters were folded and placed in polypropylene centrifuge tubes, dried for 48 h at 60 °C, and then stored in a desiccator at room temperature until analysis. Filters were digested with 4 mL of 0.2 M NaOH for 30–45 min in a water bath at 95 °C27. After digestion, samples were neutralized with 0.1 N HCl and cooled rapidly in an ice bath. Samples were centrifuged to separate out the undissolved lithogenic silica, and colorimetric analysis was performed on the supernatant. The transmittance of the samples, standards, and reverse-order reagent blanks were read at 820 nm using a Beckman DU 530 ultraviolet-visible (UV/Vis) spectrophotometer27,28.Uptake rates of carbon and nitrateSeawater samples (~0.5–1 L) were gently collected into clear polycarbonate bottles. One additional sample was collected from the 100% light depth, into a dark polycarbonate bottle, which did not allow light penetration. After the addition of the isotopic tracers (see below), bottles were placed into an acrylic incubator with constant seawater flow to maintain surface seawater temperature. Three acrylic tubes wrapped in colored and neutral density photo-film (to obtain 50, 15, and 1% of surface PAR) were used to incubate sample bottles under the same in-situ light conditions from which samples were collected. Samples from the 100% light level were placed inside the same acrylic incubator, but outside of the film-covered tubes. A LI-COR® LI-190 Quantum sensor was installed next to the incubator and continuously recorded incoming PAR for the entire incubation period. During sampling in 2010 and 2011, all experiments were performed using a shipboard incubator. For sampling from 2012 onwards, all experiments were done using an incubator on land (University of Victoria Aquatic Facility), which was connected to a seawater system maintained at local surface seawater temperature (approximately 9–12 °C depending on the time of year).Rates of C (ρC) and NO3 (ρNO3) uptake were determined using a stable isotope tracer-technique29,30 (Fig. 4). A single seawater sample from each light depth received a dual spike, with NaH13CO3 (99% 13C purity, Cambridge Isotope Laboratories) for the determination of ρC and Na15NO3 (98 + % 15N purity, Cambridge Isotopes Laboratories) for the determination of ρNO3. Isotope additions were made at approximately 10% of ambient dissolved inorganic carbon (DIC) and NO3− concentrations.Fig. 4Carbon and nitrate uptake rates in the euphotic zone of Saanich Inlet from March 11, 2010 – November 15, 2017. Left panels show depth-integrated rates (black-bars on top) and time-series profiles (filled contour/scatter plots below) of (A) carbon (ρC) and (B) nitrate (ρNO3) uptake rates. In the time-series profiles, 2012–2013 data are not interpolated due to single-depth sampling. Grey shaded regions in depth-integrated plots indicate phytoplankton growing seasons for this study (March 1st – October 30th). Right panels show monthly-averaged depth profiles for the entire 8-year period, illustrating euphotic zone seasonality for carbon and nitrate uptake. The color scale bars on the far right apply to both the total time-series vertical profiles and the 8-year seasonal plots. Sampling depths are indicated by round symbols. The year labels are positioned under the tick marks corresponding to January.Full size imageSpiked seawater samples were incubated for 24 h, except from 2010 to 2013 when the incubation period was 4 to 6 hr. After incubation, the entire sample was gently vacuum filtered onto a combusted 0.7 µm (nominal porosity) glass fibre filter. Filters were dried for 48 h at 60 °C and kept in a desiccator at room temperature until analysis. Filters were packed into pellets and sent to the Stable Isotope Facility at the University of California (UC) Davis for analysis of 13C and 15N enrichment, and total C and N content by continuous flow isotope ratio mass spectrometry and elemental analysis, respectively. For these measurements, UC Davis uses either an Elementar Vario EL Cube or Micro Cube elemental analyzer (Elementar Analysensysteme GmbH, Hanau, Germany) interfaced to either a PDZ Europa 20–20 isotope ratio mass spectrometer (Sercon Ltd., Cheshire, UK) or an Isoprime VisION IRMS (Elementar UK Ltd, Cheadle, UK).Carbon and NO3− uptake rates were calculated using Eq. 3 of Hama et al.29, and Eq. 3 and 6 of Dugdale and Wilkerson30, respectively.For samples incubated for less than 24 h, the daily C or NO3− uptake rates (ρX) were calculated using a PAR extrapolation method shown in Eq. (2):$$rho X(mu mol,{L}^{-1}da{y}^{-1})=left(rho X(mu mol,{L}^{-1}h{r}^{-1})divleft(frac{PAR,during,incubation}{Total,Daily,PAR}right)right)ast 24$$
(2)
Additionally, to account for NO3− uptake occurring under no light, ρNO3− was measured in dark bottles and this rate was added to the ρNO3− of each sample incubated for less than 24 h. The ρNO3− DARK was calculated following Eq. (3):$$rho N{O}_{3}DARK(mu mol,{L}^{-1}da{y}^{-1})=left(rho N{O}_{3}DARK(mu mol,{L}^{-1}h{r}^{-1})divleft(frac{Total,Daily,PAR-PAR,during,incubation}{Total,Daily,PAR}right)right)ast 24$$
(3)
PAR data used in Eqs. (2) and (3) came from the LI-COR® LI-190 Quantum sensor that was mounted beside the incubator. The seawater DIC value for each sample was calculated using a regression equation relating water density to DIC for Saanich Inlet31. Ambient NO3− concentrations were measured as described above. More

Monitoring sites and speciesThe monitoring survey was conducted at five sites in Fukushima Prefecture (sites 1–4 and A1) and at one site in Ibaraki Prefecture (site 5), Japan (Fig. 1). Sites 1, 2, and A1 are located in Kawauchi Village, site 3 in Otama Village, site 4 in Tadami Town, and site 5 in Ishioka City. Monitoring at sites 1–5 was started in 2011 or 2012, and site A1 was additionally monitored since 2017. The tree species, age, mean diameter at breast height, initial deposition density of 137Cs, and sampling year of each sample at each site are listed in Table 1. The dominant tree species in the contaminated area, namely, Japanese cedar (Cryptomeria japonica [L.f.] D.Don), Japanese cypress (Chamaecyparis obtusa [Siebold et Zucc.] Endl.), konara oak (Quercus serrata Murray), and Japanese red pine (Pinus densiflora Siebold et Zucc.) were selected for monitoring. Japanese chestnut (Castanea crenata Siebold et Zucc.) was supplementally added in 2017. The cedar, cypress, and pine are evergreen coniferous species, and the oak and chestnut are deciduous broad-leaved species. Sites 1 and 3 each have three plots, and each plot contains a different monitoring species. Site A1 has one plot containing two different monitoring species, and the remaining sites each have one plot with one monitoring species, giving ten plots in total.Figure 1Locations of the monitoring sites and initial deposition densities of 137Cs (decay-corrected to July 2, 2011) following the Fukushima nuclear accident in Fukushima and Ibaraki Prefectures. Open circles indicate the monitoring sites and the cross mark indicates the Fukushima Dai-ichi Nuclear Power Plant. Data on the deposition density were provided by MEXT19,20 and refined by Kato et al.21. The map was created using R (version 4.1.0)22 with ggplot2 (version 3.3.5)23 and sf (version 1.0–0)24 packages.Full size imageTable 1 Description of the sampled trees and monitoring sites.Full size tableSample collection and preparationBulk sampling of bark and wood disks was conducted by felling three trees per year at all sites during 2011–20168,25 and at sites 3–5 and A1 during 2017–2020. Partial sampling from six trees per year was conducted at sites 1 and 2 during 2017–2020 (from seven trees at site 2 in 2017) to sustain the monitoring trees. All the samples were obtained from the stems around breast height. During the partial sampling, bark pieces sized approximately 3 cm × 3 cm (axial length × tangential length) were collected from four directions of the tree stem using a chisel, and 12-mm-diameter wood cores were collected from two directions of the tree stem using an automatic increment borer (Smartborer, Seiwa Works, Tsukuba, Japan) equipped with a borer bit (10–101-1046, Haglöf Sweden, Långsele, Sweden). Such partial sampling increases the observational errors in the bark and wood 137Cs concentrations in individual trees26. To mitigate this error and maintain an accurate mean value of the 137Cs concentration, we increased the number of sampled trees from three to six. The sampling was conducted mainly in July–September of each year; the exceptions were site-5 samples in 2011 and 2012, which were collected irregularly during January–February of the following year. The collected bark pieces were separated into outer and inner barks, and the wood disks and cores were split into sapwood and heartwood. The outer and inner bark samples during 2012–2016 were obtained by partial sampling of barks sized approximately 10 cm × 10 cm from 2–3 directions on 2–3 trees per year.The bulk samples of bark, sapwood, and heartwood were air-dried and then chipped into flakes using a cutting mill with a 6-mm mesh sieve (UPC-140, HORAI, Higashiosaka, Japan). The pieces of the outer and inner bark were chipped into approximately 5 mm × 5 mm pieces using pruning shears, and the cores of the sapwood and heartwood were chipped into semicircles of thickness 1–2 mm. Each sample was packed into a container for radioactivity measurements and its mass was measured after oven-drying at 75 °C for at least 48 h. Multiplying this mass by the conversion factor (0.98 for bark and 0.99 for wood)8 yielded the dry mass at 105 °C.Radioactivity measurementsThe radioactivity of 137Cs in the samples was determined by γ-ray spectrometry with a high-purity Ge semiconductor detector (GEM20, GEM40, or GWL-120, ORTEC, Oak Ridge, TN). For measurements, the bulk and partial samples were placed into Marinelli containers (2.0 L or 0.7 L) and cylindrical containers (100 mL or 5 mL), respectively. The peak efficiencies of the Marinelli containers, the 100-mL container, and the 5-mL container were calibrated using standard sources of MX033MR, MX033U8PP (Japan Radioisotope Association, Tokyo, Japan), and EG-ML (Eckert & Ziegler Isotope Products, Valencia, CA), respectively. For the measurement of the 5-mL container, a well-type Ge detector (GWL-120) was used under the empirical assumption that the difference in γ-ray self-absorption between the standard source and the samples is negligible27. The measurement was continued until the counting error became less than 5% (higher counting errors were allowed for small or weakly radioactive samples). The activity concentration of 137Cs in the bark (whole) collected by partial sampling was calculated as the mass-weighted mean of the concentrations in the outer and inner barks; meanwhile, the concentration in the wood (whole) was calculated as the cross-sectional-area-weighted mean of sapwood and heartwood concentrations. The activity concentrations were decay-corrected to September 1, 2020, to exclude the decrease due to the radioactive decay.Trend analysesThe yearly representative values (true states) of 137Cs activity concentration in each stem part in each plot were estimated using a DLM, a state-space model in which the noise follows a normal distribution and the relationship between variables is linear. One basic DLM is the local linear trend model defined by the following equations:$$Y_{t} = mu _{t} + varepsilon _{t} ,quad quad quad varepsilon _{t} sim Normal left( {0,sigma _{varepsilon }^{2} } right)$$
(1)
$$mu_{t} = mu_{t – 1} + beta_{t – 1} + eta_{t} ,quad quad quad eta_{t} sim Normal left( {0,sigma_{eta }^{2} } right)$$
(2)
$$beta_{t} = beta_{t – 1} + zeta_{t} ,quad quad quad zeta_{t} sim Normal left( {0,sigma_{zeta }^{2} } right)$$
(3)
where Yt, μt, and βt are the observation values, level (true state), and slope, respectively, and εt, ηt, and ζt denote their corresponding noises. The subscript t is the time index. The noises εt, ηt, and ζt follow normal distributions with a mean of 0 and variances of ({sigma }_{varepsilon }^{2}), ({sigma }_{eta }^{2}), and ({sigma }_{zeta }^{2}), respectively. To detect relatively long-term trends, we employed the smooth local linear trend model28 (also called the smooth trend model, integrated random walk model, or second-order trend model), which is obtained by considering that μt and βt are driven by the same noise. The trend changes are assumed to be smoother in this model than in the local linear trend model28,29. Combining Eqs. (2) and (3), μt in the smooth local linear trend model is finally obtained as$$mu_{t} = 2mu_{t – 1} – mu_{t – 2} + eta_{t} ,quad quad quad eta_{t} sim Normal left( {0,sigma_{eta }^{2} } right)$$
(4)
The parameters μt, ({sigma }_{eta }^{2}), and ({sigma }_{varepsilon }^{2}) of each stem part in each plot were determined by Bayesian estimation with a Markov chain Monte Carlo (MCMC) method. The Bayesian estimation was performed in R (version 4.1.0)22 with the rstan package (version 2.21.2)30. Uninformative prior distributions were used for μ1, μ2, ({sigma }_{eta }^{2}), and ({sigma }_{varepsilon }^{2}). The log-transformed values of the 137Cs activity concentration (decay-corrected to September 1, 2020) were given as Yt (the observed values of multiple individuals in each year were passed via the segment function of Stan). MCMC sampling was conducted for four chains of 50,000 iterations (the first 25,000 were discarded as warmup), obtaining 100,000 MCMC samples for each parameter. The MCMC was judged to have converged when the maximum value of Rhat was less than 1.05 and the divergent transitions after warmup were fewer than 1,000 (i.e., less than 1% of the MCMC sample size). On the datasets of the outer and inner barks from site-3 oaks and all stem parts from site-A1 pines and chestnuts, the MCMC converged poorly owing to the small number of monitoring years. Thus, the temporal trends in these datasets were not analyzed (the observational data at site A1 are shown in Supplementary Fig. S1 and Table S1).To detect decadal trends rather than yearly variations, we determined the temporal trends in the true state (μ) by setting 2–4 delimiting years and examining whether μ varied significantly from one delimiting year to the next. As the delimiting years, we selected the initial and final years of monitoring and the years in which the median µ was highest (µ-max year) and lowest (µ-min year). When the µ-max year and/or the µ-min year coincided with the initial year and/or final year of monitoring, the number of delimiting years reduced from four to two or three. The trend in µ between two delimiting years was determined to be increasing and decreasing when the 95% credible interval of µ2nd delimiting year − µ1st delimiting year (obtained from the MCMC samples) was higher and lower than zero, respectively. A flat trend (no significant variation) was detected when the 95% credible interval included zero. If the 3rd and 4th delimiting years existed, the trends between the 2nd and 3rd delimiting years and between the 3rd and 4th delimiting years were determined in the same manner.The 137Cs CRs of outer bark/inner bark, heartwood/sapwood, and inner bark/sapwood were also subjected to the above trend analyses. On datasets with less than five years of monitoring, the MCMC did not converge so the trend analysis was not attempted. More

Gabor transformThe Gabor transform has rarely been used as a feature in a landscape classification OBIA approach but has been used in other OBIA processes such as fingerprint enhancement and human iris detection and for data dimensionality reduction24,29,30,31,32,33,34,35. Gabor filters are a bandpass filter applied to an image to identify texture. The different Gabor bandpass filters mathematically model the visual cortical cells of mammalian brains and thus is expected to improve segmentation and classification accuracy when compared to a human delineated and classified image26,27.Samiappan et al.36 compared Gabor filters to other texture features (grey-level co-occurrence matrix, segmentation-based fractal texture analysis, and wavelet texture analysis) within the GEOBIA process, of a wetland, using sub-meter resolution multispectral imagery. These Gabor filters performed comparably, in overall classification accuracy and Kappa coefficients, with other texture features. However, they were still outperformed by all other texture features. This study did not use any other data for analysis for determining the performance of Gabor filters when paired with data sources such as spectral, NDVI, or LiDAR36,37. Wang et al.38 paired a Gabor transformation with a fast Fourier transformation for edge detection on an urban landscape image that contained uniform textures with promising results. Su30 used the textural attributes derived from Gabor filters for classification but had similar results to Samiappan et al.36 where they found that Gabor features were one of the least useful/influential that contributed to the classification of a mostly agricultural landscape.Gabor filters are a Fourier influenced wavelet transformation, or bandpass filter, that identifies texture as intervals in a 2-D Gaussian modulated sinusoidal wave. This modulation differentiates the Gabor transform from the Fourier transform23,26. These Gabor transformed wavelets are parameterized by the angle at which they alter the image and the frequency of the wavelet. Rather than smoothing an image at the cost of losing detail through Fourier transforms or median filters, Gabor transformed images identify the repeated pattern of localized pixels and gives them similar values if they are a part of the same repeated sequence. Gabor features can closely emulate the visual cortex of mammalian brains that utilize texture to identify objects26,27. This is based on the evaluation of neurons associated with the cortical vertex that respond to different images or light profiles39. Marcelja27 identified that cortical cells responded to signals that are localized frequencies of light like what is represented by the Gabor transformations. Within the frequency domain, the Gabor transform can be defined by Eq. (1):$$Gleft(u, v;f, theta right)= {e}^{-frac{{pi }^{2}}{{f}^{2}} ({gamma }^{2}({u}^{{prime}}-f{)}^{2}+{n}^{2}{v}^{{{prime}}2})}$$
(1)

where (f) is the user-determined frequency (or wavelength); (theta) is the user-determined orientation at which the wavelet is applied to the image; (gamma) and (n) are the standard deviations of the Gaussian function in either direction23,38. These parameters define the shape of the band pass filter and determines its effect on one-dimensional signals. Daugman26, created a 2-D application of this filter in Eq. (2);$$gleft(u,vright)= {e}^{-{pi }^{2}/{f}^{2}[{gamma }^{2}{left({u}^{{prime}}-fright)}^{2}+{n}^{2}{{v}^{{prime}}}^{2}]}$$
(2)

where u’ = ucos − vsin θ θ and v’ = usin − vcos θ.In order to implement Gabor filters on multi-band spectral images, we used Matlab’s Gabor feature on the University of Iowa’s Neon high performance computer (HPC)40 which has up to 512 GB of RAM, which was necessary for processing these images. The first implementation of Gabor filters was performed on a 1610 × 687 single band pixel array (a small subset of the study area), a filter bank of 4 orientations and 8 wavelengths, on a 32 GB RAM computer, and took approximately 8 h to complete. Filter banks are a set of Gabor filters with different parameters that is applied to the spectral image and are required to identify different textures with different orientations and frequencies. By lowering the number of wavelengths from 8 to 4 on an 8128 × 8128 single band pixel array on the same machine 32 GB RAM, the processing was reduced to an hour. Using the HPC, this was further reduced to approximately 90 s using the same filter bank. Before implementing on the HPC, the original spectral image was divided into manageable subsets with overlap in order to prevent ‘edge-effect.’ These images were converted to greyscale by averaging values across all three bands33. When wavelengths become too long, they no longer attribute the textural information desired from the image and therefore add unnecessary computing time. The wavelengths that were used for the filter bank were selected as increasing powers of two starting from 2.82842712475 ((24/sqrt{2})) up to the pixel length of the hypotenuse of the input image. From this, we used only 2.82842712475, 7.0710678, 17.6776695, and 44.19417382. The directional orientation was selected as 45° intervals, from 0 to 180: 0, 45, 90, 135. These parameters were based on the reasoning outlined within Jain and Farrokhina25. More directional orientations could have been included but four were used for computational efficiency. The radial frequencies were selected so that they could capture the different texture in the landscape represented by consistent changes in pixels values within each landcover class. When frequencies are too wide or fine of a width they no longer represent the textures of the different landcover classes and thus are not included. This selection of filter bank parameters are similar or the same as other studies that look into the use of Gabor features for OBIA25,30,31.From the different combinations of parameters (four directions and four frequencies) in the Gabor Transform filter bank, sixteen magnitude response images were created from the converted greyscale three band average image. To limit high local variance within the output Gabor texture images, a Gaussian filter was applied. The magnitude response values were normalized across the 16 different bands so that a Principal Component Analysis (PCA) could be applied. The first principal component of the PCA, from these Gabor transformed images, was used for this study since it limits the computation time to process 16 separate Gabor features, in addition to the other data sources, while still retaining the most amount of information from the different Gabor response features. The Gabor band that was used for this study can be viewed in Fig. 2.Figure 2Gabor transformation. Gabor transformed image of study area derived from original image using the first principal component of all gabor outputs using the filter bank parameters. Software: ArcMap (10.x).Full size imageSegmentationFor this study, we used the watershed algorithm for the segmentation of GEOBIA, implemented by ENVI version 5.0 Feature Extraction tool, due to its ubiquitous use within GEOBIA, its ability to create a hierarchy of segmented objects, and support within the literature as a reliable algorithm37,41,39,43. The watershed algorithm can either use a gradient image or intensity image for segmentation. Based on the observed results, this study used the intensity method. The intensity method averages the value of pixels across bands. Scale, a user-defined parameter, is selected to identify the threshold that decides if a given intensity value within the gradient image can be a boundary. This allows the user to decide the size of the objects created. A secondary, user-defined, parameter defines how similar, adjacent, objects need to be before they are combined or merged. The user arbitrarily selects the parameter value based on how it reduces both under and over segmentation. The parameters selected for this study were visually chosen based on a compromise between over and under segmentation relative to the hand demarcated objects.The merging of two separate objects was based on the full lambda schedule where the user selects a merging threshold ({t}_{i, j}) which is defined by Eq. (3):$${t}_{i, j}= frac{frac{left|{O}_{i}right|cdot left|{O}_{j}right|}{left|{O}_{i}right|+ left|{O}_{j}right|}cdot {Vert {u}_{i}-{u}_{j}Vert }^{2}}{mathrm{length}(mathrm{vartheta }left({O}_{i},{O}_{j}right))}$$
(3)

where ({O}_{i}) is the object of the image, (left|{O}_{i}right|) is the area of (i), ({u}_{i}) is the average of object (i), ({u}_{j}) is the average of object (j), (Vert {u}_{i}-{u}_{j}Vert) is the Euclidean distance between the average values of the pixel values in regions (i) and (j), and (mathrm{length}left(mathrm{vartheta }left({O}_{i},{O}_{j}right)right)) is the length of the shared boundary of ({O}_{i}) and ({O}_{j}).To compare the segmentation of a riparian landscape, with and without Gabor features, we conducted segmentation on two separate sets of data. One dataset was a normalized stacked layer of NDVI and CHM (see Fig. 3) with the original multispectral image used as ancillary data; the other dataset differed only by the inclusion of the Gabor feature. For both instances, the bands were converted to an intensity image by averaging across bands rather than being converted into a gradient image for segmentation. The dataset that included the Gabor features had a scale parameter set at 30 with merge settings at 95 and 95.7 for the sub and super-objects, respectively. The dataset that did not include the Gabor features had a scale parameter of 10 with merge settings at 95.6 and 98.5 for the sub and super-objects, respectively. This resulted in the creation of 87,198 and 62,905 segments for the sub and super objects, respectively, that were created when the Gabor feature was included. 191,050 and 51,664 segments were created for the sub and super objects when the Gabor features, respectively, were not included within the segmentation process. As you will see in the next section, these segments also represent the number of training data that will be included within the supervised classification.Figure 3CHM and NDVI. LiDAR derived canopy height model (top) and normalized difference vegetation index derived from original spectral image. Software: ArcMap (10.x).Full size imageTo create a hierarchy of land cover classes, two sets of segmentation parameters needed to be selected for each dataset. One set of parameters would be used for the sub-objects within the hierarchy and the other set would be used to create super-objects. All parameters used the intensity and full lambda schedule algorithms for the watershed method. The only setting that changed between the sub and super-objects, for either dataset, was the merge parameter which helped maintain similar boundaries as much as possible. Despite this, boundaries could moderately change due to the Euclidean distance, between the pixel values of (i) and (j), changing from the merging of objects; causing ({t}_{i, j}) to cross the threshold which results in a new boundary being drawn. A representation of these results can be viewed and visually compared to the hand demarcated objects in Fig. 4.Figure 4Automated and manual segmented comparison. Juxtaposition of hand delineated, sub-objects, and super-objects for segments generated using the Gabor features. Software: ArcMap (10.x).Full size imageTraining dataThe training data, used for this study, is the transfer of class attributes from hand demarcated and classified segments to automatically segmented objects based on the majority overlap of the hand demarcated segments. Experts identified them using two different classification schemes referenced from the General Wetland Vegetation Classification System44. The 7-class scheme within this system identified objects of either being forest, marsh, agriculture, developed, open water, grass/forbs, or sand/mud. The 13-class scheme identified objects of either being agriculture, developed, grass/forbs, open water, road/levee, sand/mud, scrub-shrub, shallow marsh, submerged aquatic vegetation, upland forest, wet forest, wet meadow, and wet shrub. Not every class from the 7-class scheme will have a sub-class (i.e. developed, open water) but some do for example wet and upland forest are sub-objects of the forest class and wet meadow and shallow marsh are sub-objects of marsh. Figure 5 visually illustrates both classification schemes across the study area.Figure 5Hand delineated objects of both scales. Software: ArcMap (10.x).Full size imageENVI’s feature extraction tool calculates several landscape, spectral, and textural metrics. These attributes were used for each random forest classifier. The Gabor and Hierarchical features will be included selectively to be able to compare their contributions to the (out-of-bag) OOB classification errors. When Gabor features are included within the classification, they are computed the same way as the other image bands.Random forestThe random forest classifier was implemented in R using the random forest module45. The number of trees, that were randomly generated, was large enough (n = 250) to where the Strong law of large numbers would take effect as indicated by the decrease in the change of accuracy. The default number of variables randomly sampled as candidates at each split variable (mtry parameter) was the total number of variables divided by 3 for each dataset. R also generates two separate variable indices: mean decrease in accuracy and mean decrease Gini. Mean decrease in accuracy refers to the accuracy change in the random forest when a single variable is left out. This is a practical metric to determine the usefulness of a variable. The Gini index measures the purity change within a dataset when it is split based upon a given variable within a decision tree.The random forest classification accuracy will be based on the OOB error. The random forest algorithm trains numerous decision trees on random subsets of the training set leaving out a number of training samples when training each decision tree. The samples that are left out of each decision tree are then classified by the decision tree that they were not included within during the training step. The OOB error is the average error of each predicted bootstrapped sample across the ensemble of decision trees within the random forest algorithm.Figure 6 illustrates how the Gabor and hierarchal features were included within the classification of the super and sub-objects.Figure 6Classification procedure. Schematic flow chart illustrating how the Gabor and hierarchal features were included within the classification of the super and sub-objects. OOB classification error included in parenthesis.Full size imageHierarchical schemeTo attribute the hierarchical structure to the sub-objects, we first classified the larger segments that were created with and without the Gabor features using the broader 7-class scheme. These classified super objects were then converted to raster to calculate the majority overlap with the smaller sub-objects. This gave the sub-objects an attribute, the broader 7-class scheme, that could be used to contribute to the classification of the sub-objects with the finer 13-class scheme. This builds the hierarchical relationship between the two class schemes into the supervised classification of the sub-objects. Figure 6 illustrates how the hierarchal structure was included within two of the four sub-object’s list of features used within classification. This methodological approach aligns with O’Neill et al.21 landscape ecology principle that a super-object’s class could be a useful property in defining or predicting a sub-object. This is also different than the more common rule-based approach of iteratively classifying the landscape into smaller and smaller sub-classes22.Segmentation assessmentMost studies rely upon the accuracy assessment of their classifiers to provide support for their analysis results. However, this does not provide evidence whether a new data fusion technique improves the ability to delineate objects of interest within an image. To assess the performance of our segmented polygons, this study evaluated the segments created with and without the Gabor feature using a method highlighted in Xiao et al.37.Our segmentation results were evaluated using an empirical discrepancy measure, used frequently in image segmentation evaluation37,46,47. Discrepancy measures utilize ground truth images that represent the “correct” delineated/classified image to compare the semi-automated image results. In our study, the objects that were delineated and classified by experts from the U.S. Fish and Wildlife Service, were used as training data for our random forest classifier and as ground truth for the discrepancy measure. The discrepancy measure used the percentage of right segmented pixels (PR) in the whole image. To calculate PR, we converted the classified segmented and ground truth polygons to raster and measured the ratio of incorrect pixels to total amount of pixels which was converted to a percentage.Additionally, landscape metrics were calculated using FRAGSTATS48, an open source program commonly used for calculating landscape metrics. FRAGSTATS computed these metrics from thematic raster maps that represent the land cover types of interest. These thematic classes, used for analysis, were the classified objects at both the super and sub-object level. Since we are not attempting to compare the segmentation results for any specific class or area, we calculated metrics on a landscape level. Landscape metrics will represent the segmentation patterns for the entire study area.FRAGSTATS can calculate various metrics representing different aspects of the landscape. The metrics for analysis attempts to understand object geometry. The metrics calculated, for these analyses, were the average and standard deviation for the area (AREA), the fractal dimension index (FRAC), and the perimeter area ratio (PARA). The number of patches (NP) was also included in each result. To take a more landscape centric approach, the area weighted mean was chosen over a simple average. More

Wild animals construct various types of structures that are adaptive to their life and reproduction. For example, termites that inhabit the African savanna use soil to construct a huge mound that reaches 10 m in height; they produce hollows and holes in these mounds to allow air ventilation, thereby keeping the internal temperature constant1. In addition, prairie dogs inhabiting the North American prairie dig vertically and horizontally extending burrows in the ground that they use for shelter and rearing offspring; these burrows have multiple entrances, some of which are chimney-shaped to improve ventilation efficiency2. In the field of biomimetics, researchers apply the principles of animal-created structures in applications useful to humans3.The white-spotted pufferfish Torquigener albomaculosus (Pisces: Tetraodontidae) is a relatively small species that grows to ~10 cm in total total length (Fig. 1). Male T. albomaculosus individuals construct an intricate geometric circular structure, known as the “mystery circle,” with a diameter of 2 m in the sand of the seabed;4 the discovery of these structures has fascinated researchers and the general public worldwide. The male pufferfish digs the sand on the seabed with its fins and body while swimming straight ahead toward the centre from different directions, and a circular structure composed of radially aligned peaks and valleys was constructed. Finally, the male creates a maze-like pattern by flapping its anal fin on the bottom of the central zone4. Thus, the male completes the circular structure by himself. Furthermore, we discovered that the earliest stage of the mystery circle is composed of dozens of irregular depressions, which might function as landmarks for the formation of the radial patterns5. By accumulating observations of pufferfish behaviour, we were able to conduct a computer simulation including the swimming trajectory of the pufferfish extracted from video images wherein they constructed the circular structure. This simulation revealed that an elaborate circular geometric pattern is inevitably formed if the pufferfish repeats the digging behavior on the seabed using simple rules6. We also observed the reproductive behaviour of the pufferfish and found that they consistently breed in a semilunar cycle from spring to summer. Each male constructs a mystery circle and spawns with multiple females on the nest, and the male cares for the eggs alone until they hatch. Some of the elements of the circular structure, i.e., its size, symmetry, ornaments, and maze-like pattern, might be important factors in terms of female mate choice4,7.Fig. 1The white-spotted pufferfish Torquigener albomaculosus. Lateral view of a male (a), and male digging behaviour on the seabed while rolling up fine sand particles (b).Full size imageAlthough data on the reproductive ecology and circle-construction behaviour of these pufferfish have been collected, many questions remain. Our interdisciplinary research currently has two themes: (i) theoretical studies on the logic of 3D-structure formation of the circular structure and (ii) ethological studies on the relationship between female mate choice and the features of the structure. To advance these studies, it is essential to collect quantitative data on the circular structure. Thus, we reconstructed 3D models of six completed mystery circles using a “structure from motion” (SfM) algorithm (Fig. 2).Fig. 2“Mystery circle” constructed by a white-spotted pufferfish (Torquigener albomaculosus). 3D model displayed on a computer (a), one of the video frames used to reconstruct the 3D model (b), and a Styrofoam model output in full size created using a 3D printer and the 3D data (c) for a specific mystery circle 20160615_K13.Full size imageOn the other hand, the mystery circle constructed by the pufferfish may have potential applications in biomimetics similar to the structures constructed by termites and prairie dogs. To support the importance of its structural characteristics, it has been observed that the water passing through the valley upstream always gathers in the center of the structure, regardless of the direction of water flow4. Furthermore, particle size analysis of the sand forming the mystery circle has revealed that it has the function of extracting fine-grained sand particles from the valleys arranged radially to the outside and directing them to the center (Kawase, in prep.). The field of computational fluid dynamics, which makes full use of fluid dynamics technology, engineering knowledge, and computers, will logically clarify the characteristics of the 3D structure of the mystery circle we have reconstructed here. Shameem et al. reconstructed a 3D model of a mystery circle to explore the flow features with 2D computational fluid dynamic simulations8. Since our model has already been quantified as 3D data, computational fluid analysis can be immediately performed using this data, and the structural features of the mystery circle are expected to be applied in a wide range of fields, such as architecture and engineering, via biomimetics. More

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