Ecology

Study siteOur study site is in an intensive agricultural landscape in NW Spain known as “Tierra de Campos”, which occupies part of three out of nine provinces of Castilla-y-León region (Palencia, Valladolid, and Zamora). This area is considered the main “hot-spot” of tularemia in Spain and Southern Europe16 and is characterized by higher-than-average vole abundances during outbreaks17.Iberian hare abundance indexYearly occurrence of vole outbreaks in NW Spain between 1996 and 2020 (i.e., 1997, 1998, 2007, 2008, 2014, 2019) were identified based on reports in the news (historical reconstruction18) and more recently (from 2009 onward) using common vole abundance indices obtained from live-trapping monitoring (i.e.4,19).To study the Iberian hare population trends we used regional hunting statistics available from the regional government (Junta de Castilla-y-León, CAZDATA Project, https://medioambiente.jcyl.es/web/es/caza-pesca/cazdata-banco-datos-actividad.html [Cited 2022 Sep 23]), which included hunting records as well as the number of hunting licences from 1974 to 2020. We used the number of hunted hares divided by the number of hunting licences each year as an abundance index for hares in “Tierra de Campos” (compiling data from the provinces of Palencia, Zamora and Valladolid). CAZDATA Project is an initiative proposed by the Hunting Federation of Castilla y León, which has the support of the regional government and, more importantly, the commitment of almost 60% of the hunting societies in the community to implement a system for monitoring hunting activity. Since this information is gathered by hunters for the benefit of the hunting activity, we are confidence on its reliability to carry out the present study.
Francisella tularensis prevalence in Iberian haresWe compiled data on F. tularensis prevalence in Iberian hares from 2007 to 2016 using previously published information from a passive surveillance program carried out by the “Regional Network of Epidemiological Surveillance” (Red de Vigilancia Epidemiológica de la Dirección General de Salud Pública) of Castilla-y-León region20. This provided us with information on hare tularemia prevalence (amount of positives/number of screened individual) each year within the three provinces from “Tierra de Campos”.Statistical analysesTo study Iberian hare population trends, we calculated an index of yearly hare population instantaneous growth rate (PGR) using the hunting bag data (hare abundance index) from 1996 to 2020. Hare PGR was calculated as follows:$$PGR= lnleft(frac{{AI}_{t}}{{AI}_{t+1}}right)$$where ln stands for natural logarithm, AIt is Iberian hare abundance index on year t. and AIt+1 is the Iberian hare abundance index on year t + 1. PGRs were estimated yearly from 1996 to 2019. This dependent variable was fitted to a Generalized Linear Mixed Model using the glmmTMB function (GLMMTMB, package glmmTMB21) and a gaussian family distribution and identity link function. The categorical variable vole outbreak year (i.e., with two levels: years with (1) or without vole outbreak (0), hereafter “Vole”) and “Province” (i.e., with three levels: Palencia, Valladolid and Zamora), and their interaction were used as explanatory variables. “Year” of sampling was included as a random factor (i.e., 1996–2019). Significance of the fixed effects in the models was calculated with Type II tests using the function Anova in the car package22. We previously checked the model for overdispersion and distribution fitting using function simulateResiduals (package DHARMa23, simulations = 999). The variable PGR expresses the change between year t and t + 1. We included AI at t as a covariate in the model, in order to take into account density-dependence in hare PGR (the extent to which the abundance changes in between year t and t + 1 depends on the abundance during year t). For this to make biological sense, we rescaled the covariable AI so that it has mean equal to zero. Thus, the effect of the other predictor variables in the model (i.e., “Vole” and “Province”) was interpreted as the effect that these variables have on PGR when the abundance value is at 0. Thus, the effect of “Vole” and “Province” on PGR will be obtained by the mean value of abundance.We assessed the effect of vole outbreak years on the Iberian hare’s population PGR by running a multiple Pearson correlation (function ggscatter) between PGR and AI, considering both, PGR for all the years of the study period (i.e., 1996–2019) and only those years where vole outbreaks were detected (i.e., 1997, 1998, 2007, 2008, 2014, 2019).Finally, we tested for difference in the prevalence of F. tularensis on Iberian hare’s during years with or without vole outbreaks using a GLMMTMB21 with a binomial family distribution and a logit link function, where prevalence of F. tularensis in hares was the dependent variable, and “Vole” outbreak years and “Province” (i.e. Palencia, Valladolid and Zamora) were the responses variables. In this case, the variable “Vole” outbreak years included three levels (i.e. 0 = no vole outbreak, 1 = vole outbreak year, 2 = one year after vole outbreak), to assess if F. tularensis prevalence in hare also persist one year after a vole outbreak. “Year” of sampling was included as a random factor (i.e., 2007–2016). Due to the limited sample size, we did not include the interaction between “Vole” and “Province” to not overfit the model. We also previously checked the model for overdispersion and distribution fitting using function simulateResiduals (package DHARMa23, simulations = 999). All analysis were carried out using the R statistical computing environment24. More

Traditional ecological footprint consumption accountsTo truly reflect the ecological footprint and ecological carrying capacity of Dongying city, according to the lifestyle and consumption of Dongying city and with reference to Shandong Province Statistical Yearbook and Dongying City Statistical Yearbook, the biologically productive land is divided into arable land, forestland, grassland, water, construction land and fossil energy land, and the main consumption items of each category are shown in Fig. 3.Figure 3Traditional ecological footprint consumption accounts in Dongying city. This paper uses the carbon footprint to improve the fossil energy footprint of the traditional ecological footprint.Full size imageNPP-based correction of ecological footprint parametersThe 30 m land use of the study area was resampled to 500 m, consistent with the resolution of MOD17A3H after pre-processing with MRT and other tools. Correction of ecological footprint parameter factors in Dongying City for 2015, 2018 and 2020 based on the annual average NPP of vegetation (Table 1). This method is faster and more accurate than other methods, and the implementation of NPP calculations from the vegetation light energy use efficiency (LUE) framework to correct ecological footprint parameters is more applicable and accurate than other methods.Table 1 Average annual net primary productivity per land type in the Yellow River Delta.Full size tableYield factorThe formula for calculating the yield factor for arable land in the Yellow River Delta refers to NFA 2016:$$left{ {begin{array}{*{20}c} {Y_{j1} = frac{{Sigma A_{W} }}{{Sigma A_{N} }}} \ {A_{N} = frac{{P_{N} }}{{Y_{N} }}} \ {A_{W} = frac{{P_{N} }}{{Y_{W} }}} \ end{array} } right.$$
(1)
In Eq. (1), ({Y}_{j1}) is the yield factor of the arable land in the study area, ({A}_{N}) is the harvested area ( culture area ) of agricultural products of category (N) in the study area, ({A}_{W}) is the area required to produce an equivalent amount of this type of agricultural product based on the world average yield, ({P}_{N}) is the production of agricultural products of category (N) under the region, ({Y}_{N}) is the average yield of agricultural products of category (N) under the region, and ({Y}_{W}) is the world average production of a category of agricultural products.The NPP products from MODIS supported by remote sensing were used as the base data to correct the yield factors of woodlands and grasslands in the study area under the ecological footprint model.$$Y_{{{text{j}}2}} = overline{{NPP_{local} }} /overline{{NPP_{global} }}$$
(2)
In Eq. (2), ({Y}_{mathrm{j}2}) is the yield factor for woodland and grassland in the study area, ({NPP}_{local}) is the average annual net primary productivity of woodland and grassland in the study area in the corresponding year, and ({NPP}_{global}) is the global average NPP of woodland and grassland in the corresponding year, referring to Amthor et al.24.In addition, most of the land for construction comes from cropland, so the yield factor for construction land is the same as that for cropland25. The yield factors for the watershed were derived from the Wackernagel and Rees26 study.Balancing factorThe NPP model for provincial hectares was applied to the municipal scale. Among them, the NPP of four biologically productive lands, namely cropland, woodland, grassland and water, was weighted and summed to obtain the annual average NPP within the city area.$$overline{NPP} = frac{{mathop sum nolimits_{j} left( {A_{j} times NPP_{j} } right)}}{{mathop sum nolimits_{j} A_{j} }}$$
(3)
In Eq. (3), (overline{NPP }) is the average net primary productivity of arable land, forestland, grassland and water in Dongying, ({A}_{j}) is the area of land in category (j), and ({NPP}_{j}) is the average annual NPP of productive land in category (j).Balancing factors for arable land, woodland, grassland and water in the Yellow River Delta.$$R_{j} = frac{{NPP_{j} }}{{overline{NPP} }}$$
(4)
In Eq. (4), ({R}_{j}) is a balancing factor.The sites for construction are located in areas suitable for agricultural cultivation or directly occupy arable land, so the potential ecological productivity of urban construction land is the same as that of arable land, and therefore the equilibrium factor for construction land is equal to that of arable land27.Ecological footprint principles and improvementsEcological footprint modelEcological footprint model includes ecological footprint, ecological carrying capacity and ecological deficit. As the study area is within the city limits and the statistics have their own characteristics, adjustments have been made to the methodology for calculating the national ecological footprint accounts28. Based on the biological consumption account, the ecological footprint can be calculated for any land use type.$$EF = frac{P}{{Y_{N} }} times R_{j} times Y_{j}$$
(5)
In Eq. (5), (P) is the number of biologically productive land harvesting consumption items in a category, and ({Y}_{N}) is the average production of consumption Item (N) in the region. The ecological footprint of the construction land is measured based on the area of human infrastructure land and is equal to its ecological carrying capacity.Ecological carrying capacity is the determination of the maximum carrying capacity of an ecosystem for human activity, expressed as the sum of the biologically productive land area available in an area.$$EC = N times ec = N times sum left( {a_{j} times R_{j} times Y_{j} } right)$$
(6)
In Eq. (6), (EC) is the ecological carrying capacity per capita, and ({a}_{j}) is the per capita area of biologically productive land of category j in the region. According to the recommendations of the World Commission on Environment and Development, 12% of the ecological carrying capacity should also be deducted for biodiversity conservation. The population figures for the study area were obtained from the statistical yearbook and the seventh national census data. According to the recommendations of the World Commission on Environment and Development, 12% of the ecological carrying capacity should also be deducted for biodiversity conservation.An ecological deficit is the interpolation of the ecological footprint and ecological carrying capacity.$$ED = EF – EC$$
(7)
When (ED >0) indicates an ecological deficit, the ecological environment has exceeded the carrying capacity. Conversely, when (ED More

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Brazil’s new government aims to achieve zero deforestation in the Amazon rainforest. This welcome initiative should be extended to the Cerrado, the world’s most biodiverse woodland savannah.
Competing Interests
The authors declare no competing interests. More

The upside-down jellyfish, Cassiopea sp. produces several hydrodynamic effects capable of altering the ecosystem which it inhabits. Not only do Cassiopea produce feeding currents capable of turning over the water column above them several times per hour3, they are also capable of releasing interstitial porewater from the benthos5. The rate of porewater release, on the order of mL h−13, is capable of increasing water column NH4 levels by almost 30% under certain conditions3. In this study, we investigated two hypothetical mechanisms for this porewater release, and found that a combination of the morphology of the bell and the pulsing behavior of the jellyfish was responsible for releasing porewater from directly below the bell via a suction-pumping mechanism.The Bernoulli hypothesis4, a low-pressure zone surrounding the animal due to a velocity gradient between the substrate boundary and the incurrent flow of the Cassiopea sp. feeding current, predicted porewater release from the substrate surface surrounding the perimeter of the animal. While porewater is entrained from the perimeter of the bell into the feeding current4 lateral expulsion of porewater due to the suction pump mechanism would produce a visually similar flow of porewater. A horizontal flow of water does occur near the bottom1, but this flow is restricted to a narrow region near the bell and velocities were low compared to the vertical excurrent jet (Fig. 4). To test the effect of Bernoulli’s principle, we measured the effect on porewater release rates of an impermeable ring-shaped barrier surrounding the animal in order to inhibit benthic-pelagic fluid flux other than directly under the animal (Fig. 2A) using labeled fluorescein per the methods of Durieux et al.3, which were adapted from those of Jantzen et al.5 (Fig. 2). If the Bernoulli mechanism contributed to porewater liberation this treatment should have reduced the porewater release rate, but the release rates observed were not significantly different from the control treatment (2.23 mL h−1 ± 1.27 s.d., Fig. 2D).The suction pumping hypothesis5, a mechanism using the exumbrellar cavity as a suction pump that draws porewater vertically upward beneath the bell and then expels it laterally, would expect to see the majority of porewater released from directly under the bell of Cassiopea sp. This mechanism is supported by bell morphology5 and the appearance of deep porewater at the benthic surface of the exumbrellar cavity5. In our, an impermeable disk was placed underneath the animal to obstruct the flow predicted by the suction pump hypothesis (Fig. 2B). Additionally, we made a 6 mm perforation in the bells of the jellyfish to interfere with the ability to form the sub-ambient pressure in the exumbrellar space necessary for suction pumping to occur (Fig. 2C). Both treatments resulted in a significant decrease in porewater liberation, with flows indistinguishable from the absence of any animal (Fig. 2D), supporting the suction-pumping hypothesis.Since the suction pumping mechanism requires pressure fluctuations in the exumbrellar space, we also directly measured the water pressure below the jellyfish. The initiation of the power stroke of bell pulsation coincides with a sudden decrease in water pressure in the exumbrellar space (Fig. 3A,B) of a mean magnitude of 43.4 Pa (± 13.6 s.d.). These pressure fluctuations appear to be unaffected by animal size (Fig. 3D,E), although the rate of porewater release is known to scale with bell diameter3. Note that the muscles responsible for bell contraction in Cassiopea sp. are roughly 2-dimensional sheets13 with a thickness of one cell14 and therefore the cross-sectional area also does not scale with diameter. Our experiments were performed on smooth acrylic rather than sand, so that the conditions here were optimal for the formation of a tight seal with the bottom. However, the magnitude of this difference is likely to be small, as Cassiopea sp. produce copious amounts of mucus, which can compensate for small-scale surface roughness. In addition, the duration of each individual bell pulse is short1, so given the fine pore size of a sand or mud substrate, it is unlikely that subambient pressure would have the opportunity to dissipate enough to affect the high suction impulse produced.While not statistically significant, bell perforation did lead to data suggesting a decrease in exumbrellar pressure fluctuations (Fig. 3C), which could explain the reduction in porewater release observed (Fig. 2C). The fact that some pressure fluctuation was seen despite a complete lack of porewater release suggests that a minimum magnitude of pressure fluctuation might be necessary for suction pumping to occur. Furthermore, the effect may have been reduced by the ability of injured Cassiopea to produce copious amounts of mucus, which could have acted to minimize the impact of bell perforation. These parallel lines of reasoning firmly suggest that suction-pumping is, in fact, the dominant mechanism by which Cassiopea sp. release porewater.The suction-pumping mechanism for the release of porewater has broad-ranging ecological implications. Release rates should increase additively with population density, and the rate of bell pulsation should correlate with the rate of porewater liberation. The additive relationship to population density is important, since Cassiopea can occur at high densities of up to 100 animals m−23. Furthermore, while the Bernoulli mechanism predicted that interstitial water movement would be limited to the upper layers of the benthos, the suction pump mechanism has the potential to release porewater from deeper sediment strata. This deep flushing should expand the oxygen penetration depth downward, affecting factors such as respiration and sediment stability15. Given the fact that Cassiopea are capable of moving along the substrate5,16 this also means that the oxygen penetration depth is likely to fluctuate over time, favoring organisms that are able to adapt their metabolism or are able to relocate themselves17.Given that porewater at the field site in Long Key, Florida, from which the animals in this study were collected, has mean ammonium concentrations of 72 μM, 160 times higher than the surrounding water column11, any benthic-pelagic coupling mechanisms in this habitat could alter nitrogen dynamics, especially given the fact that many marine primary producers preferentially take up ammonium, the most reduced state of nitrogen available, as a nitrogen source18. Cassiopea sp. animal size and population densities are known to correlate with anthropogenic disturbances, and it is suggested that this is due to an increase in nutrient availability in these areas6. In addition to prey capture, Cassiopea sp. could be supplementing their nitrogen demand through the release of nutrient-rich interstitial porewater, from which Cassiopea sp. can directly absorb ammonium and other nutrients such as phosphate and trace metals5. In fact, jellyfish presence significantly reduced porewater ammonium levels near the animal5, suggesting that nutrient-rich porewater was replaced by down-welling low-nutrient surface water. The observed benthic locomotion of Cassiopea5,16 may be a mechanism to avoid remaining in locations where they have depleted this nutrient resource3. It has been reported that Cassiopea sp. affect benthic nutrient transport on a more general level, increasing ammonium uptake and decreasing nitrate uptake of the bottom sediments19. Water column nutrient levels also varied significantly between presence and absence of Cassiopea sp., and also between light and dark treatments in the presence of Cassiopea sp.20. The addition of jellyfish increased the efflux of ammonium from the benthos during the dark treatments, but reduced ammonium concentrations in the water column during light treatments20. It is entirely possible that absorption of nutrients by Cassiopea sp.5 in order to meet daytime metabolic demand resulted in the animals reducing water column ammonium concentrations in these experiments20.In addition, Cassiopea sp. have been shown to increase spatial heterogeneity of interstitial oxygen and nutrient fluxes20, making it comparable to other biogenic processes like bioturbation. Bioturbation typically oxygenates the upper layers of substrate, increasing the nitrification zone21, and also increases 3-dimensional heterogeneity of oxygen and nutrient concentrations, allowing for more complex nutrient dynamics21. The transport of interstitial porewater from specific regions under individual jellyfish could well produce a similar effect. The porewater release rates can also be compared to that of abiotic processes, such as wind-wave driven flow over sediment wave ripples, which have been shown to liberate porewater at rates of up to 140 L m−2 day−1, or three orders of magnitude greater than diffusion alone, on shallow, exposed coastlines such as beaches22. Environmental mixing would be lower in the sheltered mangrove habitats where Cassiopea sp. are found, since at our study site wind wave height was reduced from 5.4 cm in the bay to 0.07 cm in the mangroves3. In these coastal habitats, the sediment often acts as a nutrient sink, causing certain nutrients to become limiting to primary producers. Some fringe mangrove forests along coastlines in both Florida and Belize have been shown to be N-limited, for example23,24. If these nutrients are then released back into the water column, they potentially increase primary productivity in the system occupied by Cassiopea sp. Depending on the system, this could either increase production or cause eutrophication, potentially altering productivity on a local or regional scale, as has been observed when nutrients are released from the benthos by winds25 or bioturbation26.The mechanics of suction-pumping also imply that interstitial porewater release rate will correlate with bell pulse rate. Pulse rate correlates with water temperature (Fig. 5B), which would suggest that Cassiopea sp. can release greater quantities of nutrient-rich porewater during the summer months. This was confirmed by a recent study on the related species, Cassiopea medusa from Lake Macquarie, Australia8. By extension, our model suggests that pulsing, and therefore porewater release, should cease entirely below 18ºC. In fact, at our site in Lido Key, population densities of Cassiopea sp. declined rapidly once water temperatures dropped this low (Fig. 6). This same temperature of 18 °C was determined independently to be the threshold at which Cassiopea sp. polyp feeding was inhibited10. As such, it is likely that winter minimum temperatures of 18ºC represent a limiting condition on Cassiopea sp. range expansion. Studies on Cassiopea medusa, suggested thermal stress and bell degradation at 16 °C8. As global climates warm, we can expect both a poleward shift of Cassiopea sp. Range9,27 and an increase in transport rates of porewater and its associated benthic nutrients throughout this range, leading to increased productivity, and potentially exacerbating eutrophication in some regions.We determined that a suction-pumping mechanism is responsible for the interstitial porewater release by Cassiopea, suggesting that release rates are independent of population density, but affected by pulse rate. 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