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Arthropod biomass increase in spring correlates with NDVI in grassland habitat

DOI:10.1007/s00114-020-01698-7
Authors:
Mario Fernández Tizón at Spanish National Research Council
Mario Fernández Tizón
Tamara Emmenegger at Lund University
Tamara Emmenegger
Jörg Perner
Jörg Perner
Jörg Perner
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Steffen Hahn at Swiss Ornithological Institute
Steffen Hahn
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Abstract and Figures

Data from remote sensing are often used as proxies to quantify biological processes, especially at large geographical scales. The normalized difference vegetation index (NDVI) is the most frequently used proxy for primary productivity. Assuming a direct, positive interrelation between primary and secondary production in terrestrial habitats, NDVI is often used to predict food availability for higher trophic levels. However, the relationship between NDVI and arthropod biomass has rarely been tested. In this study, we analyzed extensive datasets of arthropod communities from semi-natural grasslands in central Europe to test the relationship between arthropod biomass of consumer trophic levels ("herbivores," "mixed," and "carnivores") in grassland communities and NDVI during the spring season. We found that arthropod biomass generally increased with NDVI. The same positive relationship between biomass and NDVI was observed for each individual trophic level. Cross-correlation analyses did not show statistically significant lags between the NDVI and biomass of herbivores and carnivores. All in all, our study provides correlational evidence for the positive relation of primary and secondary productivity in temperate terrestrial habitats during spring. Moreover, it supports the applicability of NDVI data as a suitable habitat-specific proxy for the food availability of insectivores during spring.
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ORIGINAL PAPER
Arthropod biomass increase in spring correlates with NDVI
in grassland habitat
Mario Fernández-Tizón
1,2
&Tamara Emmenegger
1
&Jörg Perner
3
&Steffen Hahn
1
Received: 30 April 2020 /Revised: 7 September 2020 /Accepted: 14 September 2020
#Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract
Data from remote sensing are often used as proxies to quantify biological processes, especially at large geographical scales. The
normalized difference vegetation index (NDVI) is the most frequently used proxy for primary productivity. Assuming a direct,
positive interrelation between primary and secondaryproductioninterrestrial habitats, NDVI is often used to predict food availability
for higher trophic levels. However, the relationship between NDVI and arthropod biomass has rarely been tested. In this study, we
analyzed extensive datasets of arthropod communities from semi-natural grasslands in central Europe to test the relationship between
arthropod biomass of consumer trophic levels (“herbivores,”“mixed,”and “carnivores”) in grassland communities and NDVI during
the spring season. We found that arthropod biomass generally increased with NDVI. The same positive relationship between biomass
and NDVI was observed for each individual trophic level. Cross-correlation analyses did not show statistically significant lags
between the NDVI and biomass of herbivores and carnivores. All in all, our study provides correlational evidence for the positive
relation of primary and secondary productivity in temperate terrestrial habitats during spring. Moreover, it supports the applicability of
NDVI data as a suitable habitat-specific proxy for the food availability of insectivores during spring.
Keywords Primary productivity .Secondary productivity .Proxy .Food abundance .Insects .Remote sensing
Introduction
The availability of nutritional resources can critically influ-
ence community composition and species richness
(Mittelbach et al. 2001; Ribas et al. 2003). Animals in season-
al habitats must deal with temporal variation in resource avail-
abilities caused by periodic changes in vegetation structure
(Stinson and Brown 1983) and habitat quality (Wiegand
et al. 2008). However, estimating resource availability is often
difficult to achieve, especially when large and/or remote areas
should be sampled. Thus, ecologists frequently use proxies
derived from remotely sensed data (Pettorelli et al. 2011;
Stephens et al. 2015). Their application requires knowledge
about the underlying relationship between the measured and
the predicted traits. Such interrelation is relatively easy to
establish if these traits are directly linked, as occurs between
marine primary productivity and phytoplankton abundance
(Marshall and Nesius 1996) or primary productivity and plant
biomass in terrestrial ecosystems (Scurlock et al. 2002).
However, approximations encompassing multiple trophic
levels are harder to evaluate.
In ecology, a frequently used indicator for resource approx-
imations is the normalized difference vegetation index
(NDVI), a measure of primary productivity used for many
years in remote sensing. NDVI distinguishes the reflectance
properties of the vegetation (NIR-Red)/(NIR + Red), with
NIR representing the near-infrared and red the visible red light
reflected by the surface (Myneni et al. 1995). Nowadays,
NDVI data are globally available (e.g., www.star.nesdis.
noaa.gov). The temporal and spatial resolutions of these data
have improved over time and are, therefore, ideal for the
analysis of vegetation dynamics at large scales.
Communicated by: Matthias Waltert
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00114-020-01698-7) contains supplementary
material, which is available to authorized users.
*Mario Fernández-Tizón
mario.fdez.tizon@gmail.com
1
Department of Bird Migration, Swiss Ornithological Institute, CH
6204 Sempach, Switzerland
2
Department of Biology, Geology, Physics and Inorganic Chemistry,
University Rey Juan Carlos, Móstoles, Spain
3
U.A.S. Umwelt- und Agrarstudien GmbH, 07743 Jena, Germany
https://doi.org/10.1007/s00114-020-01698-7
/ Published online: 24 September 2020
The Science of Nature (2020) 107: 42
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
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... For T. quadristriatus (spring, physical disturbance), only quadratic effects have been retained in the set of best models, this effect is therefore complicated to interpret. (Fernández-Tizón et al., 2020). The general hump-shaped effect of crops in annual, winter and spring models can result from several mechanisms. ...
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article info abstract The European range of the roller was formerly more extensive, but since the 1980s there has been a long-term decline in numbers and in range, particularly towards the north, including much of northwestern Ukraine. Our specific goals were to reconstruct the environmentally suitable range of the species in Ukraine before the 1980s, gain better knowledge on its requirements, compare the past and current suitable areas, infer the regional and environmental variables that best explain its occurrence, and quantify the overall range change in the country. For these purposes we created a database consisting of 584 findings made in Ukraine, based on a lengthy record of occurrences extending back to 1851: 203 for the period prior to 1980, 91 for records made between 1985 and 2009, and 290 records made between 2010 and 2020. 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For example, the loss of area of 'short vegetation' appears detrimental, although recent gains in this respect have favoured the bird in the Chornobyl Exclusion Zone and around, where Landsat images show the change from a previously vibrant agricultural and forestry economy, when crops have been replaced by grasslands. Threats posed to the roller by habitat and land use change are also likely to be compounded by the effects of global climate change. In summary, we suggest climate change, in particular velocity, have been responsible for shaping the contemporary home range of the European roller in Ukraine and perhaps beyond. key words Coracias garrulus, species distribution modelling, ecological niche, climate change, velocity of climate change. cite as Shupova, T., V. Tytar. 2022. Long-term monitoring of the European roller (Coracias garrulus) in Ukraine: is climate behind the changes? GEO&BIO, 23: 154-171. Резюме. 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Ми застосували підхід, заснований на принципах моделювання поширення видів (SDM), також відомий як «моделювання екологічної ніші», для ретроспективного вивчення змін ареалу сиворакши протягом історичного часу по всій України та отримання просторових прогнозів екологічно придатних для виду територій як за умов поточного клімату, так і минулого клімату, та впливу низки факторів, які за припущенням мають важливе значення для перебування сиворакши та сприяють забезпеченню достатньої бази для живлення птахів. Моделі були створені для трьох ча-сових інтервалів (до) з використанням відповідних кліматичних даних. Моделі показують скорочення екологічно придатних для птахів територій з 86 до 44%. Було розгля-нуто кілька факторів, які могли сприяти погіршенню ситуації для виду в Україні. Наприклад, втра-та площі «низькорослої рослинності» по країні є негативним фактором. Лише у Чорнобильській зоні відчуження та поблизу неї цей процес, як показують знімки Landsat, є зворотній, що сприяло птахам. 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Full-text available
  • Jun 2022
During migration, birds must stopover at refueling sites to replenish energy stores, with the rate of refueling linked to stopover length, migration speed, and the timing of critical life stages, such as breeding. Under optimal migration theory, birds are expected to maximize fuel intake and minimize stopover length (the time minimization hypothesis). Within a multi-species framework, we demonstrate that time minimization behavior is context-dependent, as refueling rate, stopover length, and departure decisions vary between seasons, among species with different ecological traits (e.g., diet and migration distance), and in response to density-dependent factors and prevailing environmental conditions. Using long-term banding data (10 years) from southwestern British Columbia, Canada, we investigated the ecological processes shaping stopover dynamics among 5 warbler (Parulidae) and 5 sparrow species (Passerellidae). Specifically, we assessed variation in fuel deposition rates (FDRs) as well as the associations between mass gain, stopover length, and departure probability. FDR was greater in insectivorous warblers during spring migration and in species migrating long distances. FDR responded positively to temperature and habitat productivity, but negatively to precipitation events, particularly for insectivorous, long-distance migrants during spring migration. Similarly, density-dependent refueling rate was only observed in insectivores and long-distance migrants during spring migration, where higher densities of foliage-gleaning insectivores were associated with a lower FDR. Stopover duration was more closely associated with body condition upon arrival and subsequent mass gain than direct environmental effects, especially during northward spring migration, providing support for time minimization and a mass threshold influencing departure decisions. These results highlight that refueling rates and stopover quality vary among species depending on their life-history strategies, with particular implications for long-distance, migratory insectivores, which may be most susceptible to climate shifts.
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Earlier nesting by generalist predatory bird is associated with human responses to climate change
Article
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Warming temperatures cause temporal changes in growing seasons and prey abundance that drive earlier breeding by birds, especially dietary specialists within homogeneous habitat. Less is known about how generalists respond to climate-associated shifts in growing seasons or prey phenology, which may occur at different rates across land cover types. We studied whether breeding phenology of a generalist predator, the American kestrel (Falco sparverius), was associated with shifts in growing seasons and, presumably, prey abundance, in a mosaic of non-irrigated shrub/grasslands and irrigated crops/pastures. We examined the relationship between remotely-sensed normalized difference vegetation index (NDVI) and abundance of small mammals that, with insects, constitute approximately 93% of kestrel diet biomass. We used NDVI to estimate the start of the growing season (SoGS) in irrigated and non-irrigated lands from 1992 to 2015 and tested whether either estimate of annual SoGS predicted the timing of kestrel nesting. Finally, we examined relationships among irrigated SoGS, weather and crop planting. NDVI was a useful proxy for kestrel prey because it predicted small mammal abundance and past studies showed that NDVI predicts insect abundance. NDVI-estimated SoGS advanced significantly in irrigated lands (β = -1·09 ± 0·30 SE) but not in non-irrigated lands (β = -0·57 ± 0·53). Average date of kestrel nesting advanced 15 days in the past 24 years and was positively associated with the SoGS in irrigated lands, but not the SoGS in non-irrigated lands. Advanced SoGS in irrigated lands was related to earlier planting of crops after relatively warm winters, which were more common in recent years. Despite different patterns of SoGS change between land cover types, kestrel nesting phenology shifted with earlier prey availability in irrigated lands. Kestrels may preferentially track prey in irrigated lands over non-irrigated lands because of higher quality prey on irrigated lands, or earlier prey abundance may release former constraints on other selective pressures to breed early, such as seasonal declines in fecundity or competition for high-quality mates. This is one of the first examples of an association between human adaptation to climate change and shifts in breeding phenology of wildlife.
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Predicting bird phenology from space: Satellite-derived vegetation green-up signal uncovers spatial variation in phenological synchrony between birds and their environment
Article
Full-text available
  • Oct 2015
Population-level studies of how tit species (Parus spp.) track the changing phenology of their caterpillar food source have provided a model system allowing inference into how populations can adjust to changing climates, but are often limited because they implicitly assume all individuals experience similar environments. Ecologists are increasingly using satellite-derived data to quantify aspects of animals' environments, but so far studies examining phenology have generally done so at large spatial scales. Considering the scale at which individuals experience their environment is likely to be key if we are to understand the ecological and evolutionary processes acting on reproductive phenology within populations. Here, we use time series of satellite images, with a resolution of 240 m, to quantify spatial variation in vegetation green-up for a 385-ha mixed-deciduous woodland. Using data spanning 13 years, we demonstrate that annual population-level measures of the timing of peak abundance of winter moth larvae (Operophtera brumata) and the timing of egg laying in great tits (Parus major) and blue tits (Cyanistes caeruleus) is related to satellite-derived spring vegetation phenology. We go on to show that timing of local vegetation green-up significantly explained individual differences in tit reproductive phenology within the population, and that the degree of synchrony between bird and vegetation phenology showed marked spatial variation across the woodland. Areas of high oak tree (Quercus robur) and hazel (Corylus avellana) density showed the strongest match between remote-sensed vegetation phenology and reproductive phenology in both species. Marked within-population variation in the extent to which phenology of different trophic levels match suggests that more attention should be given to small-scale processes when exploring the causes and consequences of phenological matching. We discuss how use of remotely sensed data to study within-population variation could broaden the scale and scope of studies exploring phenological synchrony between organisms and their environment.
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A summary of eight traits of Coleoptera, Hemiptera, Orthoptera and Araneae, occurring in grasslands in Germany
Article
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  • Mar 2015
Analyses of species traits have increased our understanding of how environmental drivers such as disturbances affect the composition of arthropod communities and related processes. There are, however, few studies on which traits in the arthropod community are affected by environmental changes and which traits affect ecosystem functioning. The assembly of arthropod traits of several taxa is difficult because of the large number of species, limited availability of trait databases and differences in available traits. We sampled arthropod species data from a total of 150 managed grassland plots in three regions of Germany. These plots represent the spectrum from extensively used pastures to mown pastures to intensively managed and fertilized meadows. In this paper, we summarize information on body size, dispersal ability, feeding guild and specialization (within herbivores), feeding mode, feeding tissue (within herbivorous suckers), plant part (within herbivorous chewers), endophagous lifestyle (within herbivores), and vertical stratum use for 1,230 species of Coleoptera, Hemiptera (Heteroptera, Auchenorrhyncha), Orthoptera (Saltatoria: Ensifera, Caelifera), and Araneae, sampled by sweep-netting between 2008 and 2012. We compiled traits from various literature sources and complemented data from reliable internet sources and the authors’ experience.
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NDVI as a predictor of canopy arthropod biomass in the Alaskan arctic tundra
Conference Paper
Full-text available
  • Feb 2015
With the physical and biological responses to arctic warming proving acute, there is a need to monitor, understand, and predict ecological responses over large spatial and temporal scales. The normalized difference vegetation index (NDVI) has been used to addresses this need, as it is a widely adopted tool for detecting and quantifying spatial and temporal dynamics of tundra vegetation cover, productivity, and phenology. Such extensive use of the NDVI to quantify vegetation characteristics suggests that it may be similarly applied to characterizing consumer communities. We developed empirical models to predict canopy arthropod biomass based on canopy-level measurements of the NDVI. We did this both across and within distinct tundra vegetation communities in the arctic tundra of Alaska. This research is a first step towards assessing the potential for datasets acquired by air and spaceborne sensors to quantify spatial and temporal dynamics in canopy arthropod biomass at landscape and regional scales. When canopy arthropod biomass was predicted with the NDVI across four growing seasons (2010 through 2013), our overall model, which included four distinct vegetation communities, explained 63% of the variance in canopy arthropod biomass. Each of our four vegetation community-specific models explained 74% (moist tussock tundra), 82% (erect shrub tundra), 84% (riparian shrub tundra), and 87% (dwarf shrub tundra) of the observed variation in canopy arthropod biomass.
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The interpretation of spectral vegetation indexes
Article
Empirical studies report several plausible correlations between transforms of spectral reflectance, called vegetation indexes, and parameters descriptive of vegetation leaf area, biomass and physiological functioning. However, most indexes can be generalized to show a derivative of surface reflectance with respect to wavelength. This derivative is a function of the optical properties of leaves and soil particles. In the case of optically dense vegetation, the spectral derivative, and thus the indexes, can be rigorously shown to be indicative of the abundance and activity of the absorbers in the leaves. Therefore, the widely used broad-band &near-infrared vegetation indexes are a measure of chlorophyll abundance and energy absorption.
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Satellite normalized difference vegetation index data used in managing Australian plague locusts
Article
The Australian Plague Locust Commission (APLC) has a mandated role in monitoring, forecasting, and managing populations of key locust species across four Australian states. Satellite normalized difference vegetation index (NDVI) imagery is used to monitor vegetation condition in locust habitat and is integrated with mapping software to support forecasting and operations within the strategic framework of APLC activities. The usefulness of NDVI data for monitoring locust habitats is tested using historical control and survey records for the Australian plague locust, Chortoicetes terminifera (Walker). In arid habitat areas, control of high-density nymphal populations was consistently associated with high and increased relative NDVI during summer and autumn, providing important information for locating possible infestations. Regression models of NDVI data and regional biogeographic factors were fitted to summer survey records of C. terminifera presence and abundance. Models identified increased vegetation greenness, measured by a one-month positive change in NDVI, as having a significant positive relationship with nymph distributions, while NDVI was significant in adult distributions. Seasonal rainfall regions and a binary habitat stratification were significant explanatory factors in all models.
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