Ecology

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All procedures involving animals were conducted in accordance with the guidelines and regulations from Institutional Animal Care and Use Committee (IACUC) of the University of Florida (protocol #201509019). Tis manuscript is reported in accordance with ARRIVE guidelines.Site descriptionThis study was carried out at the North Florida Research and Education Center, in Marianna, FL (30°46′35″N 85°14′17″W, 51 m.a.s.l). The trial was performed in two experimental years (2019 and 2020) in a greenhouse.The soil used was collected from a pasture of rhizoma peanut (Arachis glabrata Benth.) and Argentine bahiagrass (Paspalum notatum Flügge) as the main forages. Without plant and root material, only soil was placed into buckets, as described below in the bucket assemblage section. Soil was classified as Orangeburg loamy sand (fine-loamy-kaolinitic, thermic Typic Kandiudults), with a pHwater of 6.7, Mehlich-1-extratable P, K, Mg and Ca concentrations of 41, 59, 63, 368 mg kg−1, respectively. Average of minimum and maximum daily temperature and relative humidity in the greenhouse for September and November (September for beetle trial due seasonal appearance of beetles, and October and November to the Pear Millet trial) in 2019 and 2020 were 11 and 33 °C, 81%; 10 and 35 °C, 77%, respectively.Biological material determinationTo select the species of beetles, a previous dung beetle sampling was performed in the grazing experiment in the same area (grass and legume forage mixture) to determine the number of dung beetle species according to the functional groups as described by Conover et al.44. Beetles were pre-sampled from March 2017 to June 2018, where Tunnelers group were dominant and represented by Onthophagus taurus (Schreber), Digitonthophagus gazella (Fabricius), Phanaeus vindex (MacLeay), Onthophagus oklahomensis (Brown), and Euniticellus intermedius (Reiche). Other species were present but not abundant, including Aphodius psudolividus (Linnaeus), Aphodius carolinus (Linnaeus), and Canthon pilularius (Linnaeus) identified as Dweller and Roller groups, respectively. The pre-sampling indicated three species from the Tunneler group were more abundant, and thereby, were chosen to compose the experimental treatments (Fig. 4).Figure 4Most abundant dung beetle species in Marianna, FL used in the current study. Credits: Carlos C.V. García.Full size imageBeetles collection and experimental treatmentsThree species of common communal dung beetles were used: O. taurus (1), D. gazella (2), and P. vindex (3). Treatments included two treatments containing only soil and soil + dung without beetles were considered as Control 1 (T1) and Control 2 (T2), respectively. Isolated species T3 = 1, T4 = 2, T5 = 3 and their combinations T6 = 1 + 2 and T7 = 1 + 2 + 3. Dung beetles were trapped in the pasture with grazing animals using the standard cattle-dung-baited pitfall traps, as described by Bertone et al.41. To avoid losing samples due to cattle trampling, 18 traps were randomized in nine paddocks (two traps per paddock) and installed protected by metal cages, and after a 24-h period, beetles were collected, and the traps removed. Table 1 shows the number of dung beetles, their total mass (used to standardize treatments) per treatment, and the average mass per species. To keep uniformity across treatments we kept beetle biomass constant across species at roughly 1.7 to 1.8 g per assemblage (Table 1). Twenty-four hours after retrieving the beetles from the field traps, they were separated using an insect rearing cage, classified, and thereafter stored in small glass bottles provided with a stopper and linked to a mesh to keep the ventilation and maintaining the beetles alive.Table 1 Total number and biomass of dung beetles per treatment.Full size tableBuckets assemblageThe soil used in the buckets was collected from the grazing trial in two experimental years (August 2019 and August 2020) across nine paddocks (0.9 ha each). The 21 plastic buckets had a 23-cm diameter and 30-cm (0.034 m2) and each received 10 kg of soil (Fig. 5). At the bottom of the recipient, seven holes were made for water drainage using a metallic mesh with 1-mm diameter above the surface of the holes to prevent dung beetles from escaping. Water was added every four days to maintain the natural soil conditions at 60% of the soil (i.e., bucket) field capacity (measured with the soil weight and water holding capacity of the soil). Because soil from the three paddocks had a slightly different texture (sandy clay and sandy clay loam), we used them as the blocking factor.Figure 5Bucket plastic bucket details for dung beetle trial.Full size imageThe fresh dung amount used in the trial was determined based on the average area covered by dung and dung weight (0.05 to 0.09 m2 and 1.5 to 2.7 kg) from cattle in grazing systems, as suggested by Carpinelli et al.45. Fresh dung was collected from Angus steers grazing warm-season grass (bahiagrass) pastures and stored in fridge for 24 h, prior to start the experiment. A total of 16.2 kg of fresh dung was collected, in which 0.9 kg were used in each bucket. After the dung application, dung beetles were added to the bucket. To prevent dung beetles from escaping, a mobile plastic mesh with 0.5 mm diameter was placed covering the buckets before and after each evaluation. The experiment lasted for 24 days in each experimental year (2019 and 2020), with average temperature 28 °C and relative humidity of 79%, acquired information from the Florida Automated Weather Network (FAWN).Chamber measurementsThe gas fluxes from treatments were evaluated using the static chamber technique46. The chambers were circular, with a radius of 10.5 cm (0.034 m2). Chamber bases and lids were made of polyvinyl chloride (PVC), and the lid were lined with an acrylic sheet to avoid any reactions of gases of interest with chamber material (Fig. 6). The chamber lids were covered with reflective tape to provide insulation, and equipped with a rubber septum for sampling47. The lid was fitted with a 6-mm diameter, 10-cm length copper venting tube to ensure adequate air pressure inside the chamber during measurements, considering an average wind speed of 1.7 m s−148,49. During measurements, chamber lids and bases were kept sealed by fitting bicycle tire inner tubes tightly over the area separating the lid and the base. Bases of chambers were installed on top of the buckets to an 8-cm depth, with 5 cm extending above ground level. Bases were removed in the last evaluation day (24th) of each experimental year.Figure 6Static chamber details and instruments for GHG collection in the dung beetle trial.Full size imageGas fluxes measurementsThe gas fluxes were measured at 1000 h following sampling recommendations by Parkin & Venterea50, on seven occasions from August 28th to September 22nd in both years (2019 and 2020), being days 0, 1, 2, 3, 6, 12, and 24 after dung application. For each chamber, gas samples were taken using a 60-mL syringe at 15-min intervals (t0, t15, and t30). The gas was immediately flushed into pre-evacuated 30-mL glass vials equipped with a butyl rubber stopper sealed with an aluminium septum (this procedure was made twice per vial and per collection time). Time zero (t0) represented the gas collected out of the buckets (before closing the chamber). Immediately thereafter, the bucket lid was tightly closed by fitting the lid to the base with the bicycle inner tube, followed by the next sample deployment times.Gas sample analyses were conducted using a gas chromatograph (Trace 1310 Gas Chromatograph, Thermo Scientific, Waltham, MA). For N2O, an electron capture detector (350 °C) and a capillary column (J&W GC packed column in stainless steel tubing, length 6.56 ft (2 M), 1/8 in. OD, 2 mm ID, Hayesep D packing, mesh size 80/100, pre-conditioned, Agilent Technologies) were used. Temperature of the injector and columns were 80 and 200 °C, respectively. Daily flux of N2O-N (g ha−1 day−1) was calculated as described in Eq. (1):$${text{F}}, = ,{text{A}}*{text{dC}}/{text{dt}}$$
(1)
where F is flux of N2O (g ha−1 day−1), A is the area of the chamber, and dC/dt is the change of concentration in time calculated using a linear method of integration by Venterea et al.49.Ammonia volatilization measurementAmmonia volatilization was measured using the open chamber technique, as described by Araújo et al.51. The ammonia chamber was made of a 2-L volume polyethylene terephthalate (PET) bottle. The bottom of the bottle was removed and used as a cap above the top opening to keep the environment controlled, free of insects and other sources of contamination. An iron wire was used to support the plastic jar. A strip of polyfoam (250 mm in length, 25 mm wide, and 3 mm thick) was soaked in 20 ml of acid solution (H2SO4 1 mol dm−3 + glycerine 2% v/v) and fastened to the top, with the bottom end of the foam remaining inside the plastic jar. Inside each chamber there was a 250-mm long wire designed with a hook to support it from the top of the bottle, and wire basket at the bottom end to support a plastic jar (25 mL) that contained the acid solution to keep the foam strip moist during sampling periods (Fig. 7). The ammonia chambers were placed installed in the bucket located in the middle of each experimental block after the last gas sampling of the day and removed before the start of the next gas sampling.Figure 7Mobile ammonia chamber details for ammonia measurement in dung beetle trial. Adapted from Araújo et al.51.Full size imageNutrient cyclingPhotographs of the soil and dung portion of each bucket were taken twenty-four hours after the last day of gas flux measurement sampling to determine the dung removal from single beetle species and their combination. In the section on statistical analysis, the programming and statistical procedures are described. After this procedure, seeds of pearl millet were planted in each bucket. After 5 days of seed germination plants were thinned, maintaining four plants per bucket. Additionally, plants were clipped twice in a five-week interval, with the first cut occurring on October 23rd and the second cut occurring on November 24th, in both experimental years. Before each harvest, plant height was measured twice in the last week. In the harvest day all plants were clipped 10 cm above the ground level. Samples were dried at 55 °C in a forced-air oven until constant weight and ball-milled using a Mixer Mill MM 400 (Retsch, Newton, PA, USA) for 9 min at 25 Hz, and analyzed for total N concentration using a C, H, N, and S analyzer by the Dumas dry combustion method (Vario Micro Cube; Elementar, Hanau, Germany).Statistical analysisTreatments were distributed in a randomized complete block design (RCBD), with three replications. Data were analyzed using the Mixed Procedure from SAS (ver. 9.4., SAS Inst., Cary, NC) and LSMEANS compared using PDIFF adjusted by the t-test (P  More

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Study site, tree selections, and drought-simulation experimentThis research was performed in Guangzhou (22°26′-23°56′N, 112°57′-114°03′E), which is a core city located in subtropical zones. With an area of 7434.4 km2 and a population of 18.87 million, Guangzhou’s urbanization rate has reached 86.46%. To cope with multiple environmental challenges, several urban-forest nurseries were established to cultivate and introduce various tree species. Among them, we selected the one in Tianhe District as our study site. This nursery was not only abundant with native and exotic tree species but also equipped with similar edatope in cities, which was ideal for our research.Tilia cordata Mill. (Tc) and Tilia tomentosa Moench (Tt), originating from the west of Britain and southeast of Europe, were common urban tree species planted in European cities. Based on their performance in providing ecological and landscape functions, these two tree species were considered to be introduced for urban greening. Therefore, Tilia cordata Mill. (Tc) and Tilia tomentosa Moench (Tt) were selected as our objectives, which were investigated for their growth and ecosystem services to evaluate their adaption in Guangzhou. In addition, a native tree species Tilia miqueliana Maxim (Tm) was also implemented concurrent measurement as a comparison.For each of the three surveyed tree species, ten trees with a diameter at breast height (DBH) around 5.5 cm and tree height around 2.5 m were chosen for our experiment, which were thought to possess similar initial statuses. To investigate the impact of drought on the growth and ecosystem services of the three selected tree species, a controlled experiment was launched from January to December in 2020. For each tree species, five trees were planted in the common environment as the controlled group, while the other five trees were under the precipitation-exclusion installation (PEI) as the drought-simulation group. Consisting of several water-proof tents, PEI was adequately large and could completely prevent trees from obtaining rainfalls, which created a precipitation-exclusive environment to simulate an enduring drought event within the whole research period (Fig. 1).Figure 1Schematic diagram of the drought simulation experiment for the three surveyed tree species.Full size imageEnvironmental monitoring systemsClimatic data were sampled every 10 min with a weather station (WP3103 mesoscale automatic weather station, China) located at an unshaded site in the nursery. The data were stored in the logger and copied to our laboratory to produce daily or monthly data. All the climatic variables, including photosynthetically active radiation (PAR, µmol m-2 s-1), wind speed (m s-1), precipitation (mm), and air temperature (°C) were calculated from January to December in 2020.For volumetric soil water content (%; VWC), the HOBO MX2307 system (Onetemp, Adelaide, Australia), placed in a shaded box in the nursery, was applied for all the three tree species from both the controlled and drought-simulation groups. For each individual tree, the sensing probe was inserted horizontally at the depths of 30 cm and located 20 cm in the northern direction from the tree stems. Based on the daily readings, monthly means were calculated from January to December in 2020.Measurement of above-ground growthTo investigate the above-ground growth of the three tree species from both the controlled and drought-simulation groups, their DBH (diameter at breast height, cm), tree height (m), and LAI (leaf area index) were measured at the beginning of each month in 2020. DBH was measured with the help of a caliper (Altraco Inc., Sausalito, California, USA), and their tree heights were measured using a standard tape. The crown analytical instrument CI-110 (Camas, Washington State, USA) was used to capture an accurate image of tree crowns and calculate LAI. Sufficient numbers of points were measured and recorded to describe each tree’s average crown shape. The software FV2200 (LICOR Biosciences, Lincoln, NE) helped compute each tree’s crown width and crown area.Measurement of below-ground growthFine root coring campaigns were launched for all the trees of the three tree species from both the controlled and drought treatment groups every three to four months, i.e., in February, May, September, and December. Although the coring campaign might damage part of the roots, the fine roots obtained each time were a mere portion of the whole root system, not affecting the general development of trees’ underground processes. For every individual tree, two 30-cm soil cores were applied in each direction of north, south, east, and west, of which one was located at 20 cm to the trunk (paracentral roots) and the other one was located at 40 cm (outer roots). In addition, the soil samples were evenly divided into three horizons which were 0–10 cm (shallow layer), 10–20 cm (middle layer), and 20–30 cm (deep layer). Then a sieve with 2-mm mesh size was used to filter all the fine roots. The fine roots were washed carefully to remove the adherent soils and dried in an oven at 65 ℃ for 72 h. Finally, all the samples were weighed using a balance with an accuracy of four decimal places to obtain the dry weight. The fine root biomass at different depths was calculated using the dry weight divided by the cross-sectional area of the auger20.Model’s simulation of ecosystem servicesThe process-based model City-Tree was used to predict the ecosystem services of the three tree species from both the controlled and drought-simulation groups23. The model required the data of tree growth parameters including tree height, DBH, and crown area together with environmental conditions such as edaphic and climatic data24. In this research, cooling, evapotranspiration and CO2 fixation of the three surveyed tree species in the controlled and drought-treatment groups were simulated at the end of 2020.The actual evapotranspiration eta was calculated from the potential evapotranspiration using fetp[t], Tilia’s factors fetp[t], and the reduction factor fred:$${mathrm{et}}_{mathrm{a}}={mathrm{f}}_{mathrm{red}}*{mathrm{f}}_{mathrm{etp}}left[mathrm{t}right]*{mathrm{et}}_{mathrm{p}}$$The process of tree’s evapotranspiration (etp) was calculated on the basis of SVAT algorithm together with Penman formula in the module on water balance as below:$${mathrm{et}}_{mathrm{p}}=left[mathrm{s }/ left(mathrm{s}+upgamma right)right]*left({mathrm{r}}_{mathrm{s}}-{mathrm{r}}_{mathrm{L}}right) /mathrm{ L}+left[1-mathrm{s }/ left(mathrm{s}+upgamma right)right]*{mathrm{e}}_{mathrm{s}}*mathrm{f }left({mathrm{v}}_{mathrm{u}}right)$$with γ: psychrometric constant in hPa K−1; s: the slope of the saturation vapour pressure curve in hPa K−1; rs: short wave radiation balance in W m−2; rL: long-wave radiation balance in W m−2; L: specific evaporation heat in W m−2 mm−1 d; es: saturation deficit in hPa; f (vu): ventilation function with vu being the daily average wind speed in m s−1.Within the module cooling, the energy needed for the transition of water from liquid to gaseous phase was calculated based on the crown area (CA) and the transpiration eta sum:$${mathrm{E}}_{mathrm{A}}= {mathrm{et}}_{mathrm{a}}*mathrm{CA}-left({mathrm{L}}_{mathrm{O}}* -0.00242*mathrm{temp}right) / {mathrm{f}}_{mathrm{con}}$$with EA: energy released by a tree through transpiration (kWh tree-1), LO: energy needed for the transition of the 1 kg of water from the liquid to gaseous phase = 2.498 MJ (kgH2O)-1 and temp = temperature in ℃, fcon: 0.5.The calculation of new assimilation in the module of photosynthesis and respiration was on the basis of the approach of Haxeltine and Prenticem25. The model assumed that 50% of the incoming short-wave radiation is photosynthetic active radiation (PAR). Using the LAI and a light extinction factor of 0.5, the radiation amount of 1 m2 leaf area can be estimated based on an exponential function according to the Lambert–Beer law. This way, the gross assimilation per m2 leaf area as the daily mean of the month can be derived from:$${text{A}} = {text{d}}*{{left[ {left( {{text{J}}_{{text{p}}} + {text{J}}_{{text{r}}} – {text{sqrt}} left( {left( {{text{J}}_{{text{P}}} + {text{J}}_{{text{r}}} } right)^{2} – 4*uptheta *{text{J}}_{{text{p}}} *{text{J}}_{{text{r}}} } right)} right)} right]} mathord{left/ {vphantom {{left[ {left( {{text{J}}_{{text{p}}} + {text{J}}_{{text{r}}} – {text{sqrt}} left( {left( {{text{J}}_{{text{P}}} + {text{J}}_{{text{r}}} } right)^{2} – 4*uptheta *{text{J}}_{{text{p}}} *{text{J}}_{{text{r}}} } right)} right)} right]} {left( {2*uptheta } right)}}} right. kern-0pt} {left( {2*uptheta } right)}}$$with A: gross assimilation [g C m−2 d−1]; d: mean day length of the month [h]; Jp: reaction of photosynthesis on absorbed photosynthetic radiation [g C m−2 h−1]; Jr: rubisco limited rate of photosynthesis [g C m−2 h−1]; θ: form factor = 0.7.Jp was defined as a function of the photosynthetic active radiation PAR in mol m−2 h−1 and the efficiency of carbon fixation per absorbed PAR [g C mol−1].$${text{J}}_{{text{p}}} = {text{c}}_{{text{p}}} {text{*PAR}}$$$${text{c}}_{{text{p}}} = alpha *left( {{text{p}}_{{{text{ci}}}} – {text{r}}} right){ /}left( {{text{p}}_{{{text{ci}}}} – {text{r}}} right)*gamma *{text{m}}_{{{text{co}}_{2} }} *{text{i}}left[ {text{t}} right]$$with α: intrinsic quantum efficiency for CO2 uptake = 0.08; pci: partial pressure of the internal CO2 [Pa]; r: CO2 compensation point [Pa]; ϒ: species dependent adjustment function for tree age; m CO2: molecular mass of C = 12.0 g mol−1; i[t]: influence of temperature on efficiency.Net assimilation AN [g C m−2 d−1] was then derived from the gross assimilation A and the dark respiration Rd by:$${text{A}}_{{text{N}}} = {text{A}} – {text{R}}_{{text{d}}}$$$${text{R}}_{{text{d}}} =upbeta *{text{V}}_{{text{m}}}$$where Vm was calculated as:$${text{V}}_{{text{m}}} = {1 mathord{left/ {vphantom {1 upbeta }} right. kern-0pt} upbeta } * {{{text{c}}_{{text{p}}} } mathord{left/ {vphantom {{{text{c}}_{{text{p}}} } {{text{c}}_{{text{r}}} * {text{PAR}} * left[ {left( {2uptheta – 1} right) * beta * {{text{d}} mathord{left/ {vphantom {{text{d}} {{text{d}}_{max } }}} right. kern-0pt} {{text{d}}_{max } }} – left( {2uptheta *upbeta *{{text{d}} mathord{left/ {vphantom {{text{d}} {{text{d}}_{max } }}} right. kern-0pt} {{text{d}}_{max } }} – {text{c}}_{{text{r}}} } right)*varsigma } right]}}} right. kern-0pt} {{text{c}}_{{text{r}}} * {text{PAR}} * left[ {left( {2theta – 1} right) * beta * {{text{d}} mathord{left/ {vphantom {{text{d}} {{text{d}}_{max } }}} right. kern-0pt} {{text{d}}_{max } }} – left( {2theta *upbeta *{{text{d}} mathord{left/ {vphantom {{text{d}} {{text{d}}_{max } }}} right. kern-0pt} {{text{d}}_{max } }} – {text{c}}_{{text{r}}} } right)*varsigma } right]}}$$By multiplying AN, the number of days and the total leaf area, the entire monthly net assimilation of the tree can be obtained. In this study, we assumed a fixed share of 50% as respiration based on the gross primary production that the resulting net primary production NPP was transformed in the content of fixed carbon by multiplying the value with the carbon conversion factor 0.524.$${mathrm{Carbon}}_{mathrm{fix}}=0.5*mathrm{NPP}$$Statistical analysesThe software package R was used for statistical analysis. To investigate the differences between means, two-sampled t-test and analysis of variance (ANOVA) with Tukey’s HSD (honestly significant difference) test were used. All the cases, the means were reported as significant when P  More

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