Ecology

Dataset of food flow networksWe derive annual, intranational food flow networks for the USA using the Freight Analysis Framework version 4 (FAF4) database30. The derived networks are for different food sectors and include all metropolitan areas in the USA. The FAF4 database consists of annual commodity flows during 2012−2015 for 115 geographic areas in the USA and 43 different sectors. We focus on the following four food sectors in the FAF4 database: crops, live animals, animal feed and meat. The 115 geographic areas in the FAF4 database cover the entire contiguous USA, including 69 metropolitan statistical areas and 46 remainders of states (the remainder is the area of a state that is not part of a FAF4 metropolitan area).To obtain food flows for all metropolitan areas in the USA, we disaggregate the FAF4 database from 115 to 329 areas (Supplementary Fig. 4), out of which 284 are metropolitan or combined statistical areas (120 metropolitan and 164 combined statistical areas). The disaggregation is performed using different socioeconomic and agricultural-related variables as attractors of supply and demand. For each food sector, a flow with origin o and destination d in the FAF4 database is disaggregated to a metropolitan-level flow with origin o′ and destination d′ using a disaggregation variable a as the best attractor of supply or demand.The disaggregation is performed in two stages. In the first stage, the supply U of each FAF4 remainder of state is disaggregated to include all the metropolitan areas in that remainder of state as follows:$${U}_{{o}^{{prime} }d}^{c}=frac{{U}_{od}^{c}}{{a}_{o}}times {a}_{{o}^{{prime} }},$$
(3)
where ({U}_{{o}^{{prime} }d}^{c}) (in tons per year) is the disaggregated supply for food sector c in origin o′ that satisfies demand at the FAF4 destination d, ({U}_{od}^{c}) (in tons per year) is the FAF4 food flow for sector c between areas o and d, and ({a}_{{o}^{{prime} }}) and ao are the attractor variables for the new origin o′ and FAF4 origin o, respectively. In the second stage, ({U}_{{o}^{{prime} }d}^{c}) is further disaggregated into demand E using:$${E}_{{o}^{{prime} }{d}^{{prime} }}^{c}=frac{{U}_{{o}^{{prime} }d}^{c}}{{a}_{d}}times {a}_{{d}^{{prime} }},$$
(4)
where ({E}_{{o}^{{prime} }{d}^{{prime} }}^{c}) (in tons per year) is the demand at destination d′ for food sector c supplied by origin o′, while ({a}_{{d}^{{prime} }}) and ({a}_{d}) are the attractor variables at the disaggregated destination d′ and FAF4 destination d, respectively.The FAF4 database includes food flow data at both the state level (48 states) and metropolitan level (115 areas including 69 metropolitan areas). Prior to performing the disaggregation, we jointly use the FAF4 state data and the FAF4 metropolitan data to select the best performing attractor variables. That is, we first use equations (3) and (4) to disaggregate the FAF4 state-level data to the metropolitan-level for the metropolitan and remainder-of-state areas in FAF4. By comparing the performance of our disaggregated flow data against the empirical FAF4 metropolitan-level data, we select the best attractor variable for each food sector. The following attractor variables are considered: population47, employment48, wages48, number of establishments48 and cropland area49. These variables are selected on the basis of previous analysis and data availability50.To assess the performance of the attractor variables, we use the Pearson correlation coefficient between the empirical FAF4 flows and the disaggregated flows for the metropolitan areas and remainder-of-state areas in FAF4 (Extended Data Fig. 3). The performance is high with correlation values greater than 0.87 and an average of 0.95. Using the best-performing disaggregation variables, we build the food flow networks employed in this study. The nodes in the networks represent metropolitan and remainder-of-state areas, and the weighted links represent annual food flows during 2012−2015 for crops, live animals, feed and meat (Supplementary Fig. 5).The FAF4 metropolitan and remainder-of-state areas we used to select the attractor variables span a wide range of populations, cropland areas, and number of establishments, since these FAF4 areas include the largest cities in the USA and a broad range of medium-size cities. The values of the attractor variables used in the disaggregation are within the ranges implied by the FAF4 metropolitan data (Supplementary Fig. 6), indicating that the variables are reliable. The exception to this is population, which is only used to disaggregate meat demand. Population, however, has a high disaggregation performance with a correlation coefficient of 0.97 (Extended Data Fig. 3). In addition, the use of population to disaggregate meat demand is consistent with previous scaling results for metropolitan areas in the USA51 that have shown that metropolitan-level variables that are related to resource consumption scale approximately linearly with population.Food inflows supply chain diversityTo determine annual supply chain diversity, we extract the annual food buyer–supplier subgraph of each city and food sector from the food flow networks19. We refer to each of these subgraphs as a food system. The food buyer–supplier subgraph of a city i consists of all the supply chain interactions with its trading partners or neighbours j for a specific food sector. Our measure of supply chain diversity is based on the notion of functional distance52. We compute the functional distance d between i and any of its trading partners j by combining five different indicators: physical distance, climate correlation, urban classification, economic specialization and network modularity. The indicators are described below in the ‘Functional distance indicators’ section of the Methods. We also perform statistical analyses to evaluate the influence of the attractor variables on these indicators (Methods). The indicators represent stable characteristics of cities and therefore tend to remain fairly constant during our study period.The functional distance ({d}_{ij}^{r}) for an indicator r between any pair of connected nodes (i,j) is calculated as$${d}_{ij}^{r}={N}^{-1}|{r}_{k}-{r}_{i}|,$$
(5)
where the normalization constant N is determined as the maximum value of (|{r}_{k}-{r}_{i}|) between any node k in the network and i. In equation (5), ({d}_{ij}^{r}=0) for functionally similar nodes and ({d}_{ij}^{r}=1) for dissimilar nodes.For each city’s buyer−supplier subgraph and food sector, any pair of connected nodes has 5 different functional distance indicators associated with it. To combine these distance indicators into a single measure, we calculate the average functional distance indicator (langle {d}_{ij}^{r}rangle ) as the arithmetic average of the 5 functional distance indicators for any pair (i, j) of connected nodes. We use the discrete probability distribution of food inflows binned by (langle {d}_{ij}^{r}rangle ) categories, together with Shannon entropy53, to calculate the supply chain diversity ({D}_{i,c}^{t}) of node i and sector c at year t:$${D}_{i,c}^{t}=frac{-{sum }_{k=1}^{K}{Y}_{i,c}^{t}(k)mathrm{ln},{Y}_{i,c}^{t}(k)}{log ,K}.$$
(6)
For sector c and year t, ({Y}_{i,c}^{t}(k)) is the proportion of food inflows to node i within bin k. The k bin is obtained by binning all the (langle {d}_{ij}^{r}rangle ) values for node i into a total number of K bins.({D}_{i,c}^{t}) is sensitive to the total number of bins K. Thus, for each node in our food flow networks, we tested the sensitivity of ({D}_{i,c}^{t}) to the total number of bins K. For K = 15, D values stabilize (Supplementary Fig. 7); therefore, we used 15 bins when performing all calculations of functional diversity.Functional distance indicatorsThe average functional distance between a city and its trading partners is based on the following five indicators:

(1)

Physical distance indicator (PDI). The PDI is obtained by calculating the Euclidean distance from the centroid of each geographic area to the centroid of all other areas. The geometric centroids of all geographical areas are calculated using the GIS software ArcMap (https://desktop.arcgis.com/en/arcmap/).

(2)

Climate indicator (CI). To account for different climates in cities across the USA, the Palmer Drought Severity Index (PDSI) is used54. The monthly PDSI is obtained from the National Oceanic and Atmospheric Administration for the years 1895−2015 at the climate division geographic level. An area-weighted average is performed to aggregate the PDSI data to the metropolitan level. The CI is obtained by calculating the monthly correlation between an area and all other areas.

(3)

Urban classification indicator (UCI). To identify the urbanization level of a geographical area, the Urban-Rural Classification indicator of the National Center for Health Statistics is employed55. This indicator classifies counties using a scale from 1 to 6, where a value of 1 indicates the county is highly rural and a value of 6 means highly urban. The UCI is obtained at the metropolitan level using an area-weighted average of the county-level values.

(4)

Network modularity indicator (NMI). This indicator identifies geographical areas (network nodes) that belong to the same community. A community is a group of nodes whose strength interactions are stronger than with the rest of the network. To identify the network’s communities, we aggregate the flows from the four food sectors (crops, live animals, feed and meat) into a single-layer network. The communities are identified by maximizing the modularity measure of Newman56,57 using the greedy optimization algorithm of Blondel et al.58,59. Network nodes that lie in the same community are assigned a NMI of 1 and 0 otherwise.

(5)

Economic specialization indicator (ESI). Each geographical area is assigned a score based on its dominant economic supply sector. Supply is quantified using the FAF4 intranational commodity flows30. Areas with a dominant meat sector are assigned an ESI of 1, crops an ESI of 2, fruits and vegetables an ESI of 3, animal feed an ESI of 4, live animals an ESI of 5, milled grains an ESI of 6, and industrial products an ESI of 7.

Probabilities of food supply chain shockThe annual probability of food supply chain shock is calculated as the probability that food inflows to a city fall below a percentage of the average inflows for that city during 2012−20158. To compute this probability, we group all nodes from the 4 food flow networks (1,221 observations) into 6 diversity bins ordered from lowest to highest functional diversity D. The bin size is selected to obtain bins with similar number of observations, approximately 204 observations in each bin. For each city i and food sector c in a bin, we calculate the food supply chain shock ({S}_{i}^{c}) as$${S}_{i}^{c}=left[1-frac{min({I}_{i}^{c})}{langle {I}_{i}^{c}rangle }right]times 100,$$
(7)
where ({I}_{i}^{c}) is the time series of total food inflows to node i for sector c during 2012−2015, and ({rm{min }}({I}_{i}^{c})) and (langle {I}_{i}^{c}rangle ) are the minimum and average values of the time series ({I}_{i}^{c}), respectively.For each diversity bin b, we count the number of observations nb that meet the criteria ({S}_{i}^{c} > s) for (sin {3,4,5,ldots ,15}), with s being the shock intensity threshold. The probability of a food supply shock S being greater than s in bin b is calculated as:$${P}_{b}(S > s)=frac{{n}_{b}}{{N}_{b}},$$
(8)
where Nb is the total number of observations in bin b. Thus, for each shock intensity s, we obtain a set of probabilities of food supply chain shock,$$P(S > s)={P}_{b}(S > s),{rm{for}},b={1,ldots ,6}.$$
(9)
Furthermore, we adapt equations (8) and (9) to calculate the probability of a food supply chain shock S being greater than s, P′(S > s), under co-occurrence conditions. We define co-occurrence as any city that experiences a shock to 2 or more food sectors during 2012−2015. With this definition, P′(S > s) is calculated in a fashion similar to that described above. We bin the network’s nodes into 6 groups from lowest to highest diversity and determine the percentage of food supply chain shock with equation (7). Letting ({n}_{b}^{{prime} }) be the total number of cities for which ({S}_{i}^{c} > s,) holds for 2 or more food sectors, the probability of a food supply chain shock S being greater than the shock intensity s in bin b is now$${P}_{b}^{{prime} }(S > s)=frac{{n}_{b}^{{prime} }}{{N}_{b}^{{prime} }},$$
(10)
where ({N}_{b}^{{prime} }) is the total number of cities in bin b. Thus, under co-occurrence conditions, the new set of probabilities for each shock intensity s is$$P{prime} (S > s)={P}_{b}^{{prime} }(S > s),{rm{for}},b={1,ldots ,6}.$$
(11)
Statistical analysesWe use the disaggregated food flow data to calculate both the probability of food supply chain shock and supply chain diversity. Therefore, we perform two complementary analyses to test whether the attractor variables used in the disaggregation are causing a circularity issue in the empirical relationship between the probability of food supply chain shock and supply chain diversity. For the first analysis, we determine the Pearson correlation between the functional distance indicators (PDI, CI, UCI, NMI and ESI) and the attractor variables (Supplementary Fig. 8). We find that the attractor variables are weakly correlated with the functional distance indicators (Supplementary Table 1). For the second analysis, we determine the Pearson correlation between the food supply chain shock intensities and attractor variables for the 4 food sectors (Supplementary Fig. 9). The attractor variables are also weakly correlated with the food supply chain shock intensities (Supplementary Table 2). Thus, circularity is not unduly influencing the empirical relationship between the probability of shock and supply chain diversity.We also evaluate whether the empirical relationship between the probability of food supply chain shock and supply chain diversity is driven by the disaggregation of the original FAF4 data. For this, we recalculate the probability of shock and supply chain diversity using the FAF4 data. For the FAF4 data, the probability of shock also declines with rising supply chain diversity (Supplementary Fig. 10), similar to the reduction observed using the disaggregated food flow data (Fig. 1a), suggesting that the latter data are not driving the relationship.Furthermore, we test whether the relationship between the probability of food supply chain shock and supply chain diversity holds for different demand levels. To control for demand, we stratify all the data into low, medium and high demand levels using population or food inflows as proxies for demand. For both stratifications, the bounds are chosen so that each level has approximately the same number of data points. Using the stratified data, we recalculate the Pearson correlation between the probability of shock at 3%, 5%, 10% and 15% shock intensities and supply chain diversity for each level of population or food inflows (Supplementary Table 3). We find that the relationship between the probability of food supply chain shock and supply chain diversity holds for these different demand levels (Supplementary Table 3). Using the same exponential model in equation (1) to fit the relationship for the stratified data (Supplementary Fig. 11), we determine the exponential model parameters ks and D0,s for each demand level (Extended Data Table 6). These parameters fall within the 95% confidence interval of the parameters of the exponential model in the main text (Extended Data Table 1), indicating that the model is robust.We perform two different sensitivity analyses to assess the influence of the five distance indicators on the empirical relationship between the probability of food supply chain shock and supply chain diversity. The first analysis compares single-indicator diversity measures against the multi-indicator diversity measure calculated using all 5 indicators. Five different single-indicator diversity measures are compared, one measure for each of the 5 indicators: PDI, CI, UCI, NMI and ESI. For the second sensitivity analysis, we leave out one indicator at a time to calculate diversity using the 4 remaining indicators, which results in another 5 different diversity measures. The diversity measures for the sensitivity analyses are all calculated following the approach in the ‘Food inflows supply chain diversity’ section of the Methods. To perform the sensitivity analyses, we plot the empirical relationship between the probability of food supply chain shock and each diversity measure (Supplementary Figs. 12 and 13), and calculate the Pearson correlation of the data (Extended Data Table 7). The correlation coefficients are used to quantify the influence of the distance indicators on the relationship between the probability of food supply chain shock and supply chain diversity (Extended Data Table 7). The probabilities of food supply chain shock are calculated following the approach in the ‘Probabilities of food supply chain shock’ section of the Methods. We find that the five indicators have a varied influence on the relationship between the probability of food supply chain shock and supply chain diversity (Extended Data Table 7). The inclusion of all 5 indicators, however, in the supply chain diversity measure increases the Pearson correlation between the probability of food supply chain shock and supply chain diversity (Extended Data Table 7). More

1.Pontier, D. et al. Postnatal growth rate and adult body weight in mammals: A new approach. Oecologia 80, 390–394 (1989).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
2.Dmitriew, C. M. The evolution of growth trajectories: What limits growth rate?. Biol. Rev. 86, 97–116 (2011).PubMed 
Article 
PubMed Central 

Google Scholar 
3.Gotthard, K., Nylin, S. & Wiklund, C. Adaptive variation in growth rate: Life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99, 281–289 (1994).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
4.Arendt, J. D. Adaptive intrinsic growth rates: An integration across taxa. Q. Rev. Biol. 72, 149–177 (1997).Article 

Google Scholar 
5.Gaillard, J. M. et al. Variation in growth form and precocity at birth in eutherian mammals. Proc. R. Soc. B Biol. Sci. 264, 859–868 (1997).ADS 
CAS 
Article 

Google Scholar 
6.Gillooly, J. F., Charnov, E. L., Geoffrey, B. W., Savage, V. M. & James, H. B. Effects of size and temperature on developmental time. Nature 417, 70–73 (2002).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
7.Brown, J. H., Gillooly, J. F., Allen, P. A., Savage, V. M. & Geoffrey, B. W. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).Article 

Google Scholar 
8.Roff, D. A. The Evolution of Life Histories: Theory and Analysis (Sinauer Associates, 1992).9.Stearns, S. C. The Evolution of Life Histories (Oxford University Press, 1992).10.Ferré, P., Decaux, J. F., Issad, T. & Girard, J. Changes in energy metabolism during the suckling and weaning period in the newborn. Reprod. Nutr. Dev. 26, 619–631 (1986).PubMed 
Article 
PubMed Central 

Google Scholar 
11.Gadgil, M. & Bossert, W. H. Life history consequences of natural selection. Am. Nat. 104, 1–24 (1970).Article 

Google Scholar 
12.Lee, A. H., Huttenlocker, A. K., Padian, K. & Woodward, H. N. Analysis of growth rates. In Bone Histology of Fossil Tetrapods (eds Padian, K. & Lamm, E.-T.) 217–264 (University of California Press, 2013).13.Amprino, R. L. structure du tissu osseux envisagée comme expression de différences dans la vitesse de l’accroisement. Arch. Biol. (Liege) 58, 315–330 (1947).
Google Scholar 
14.Nacarino-Meneses, C. & Köhler, M. Limb bone histology records birth in mammals. PLoS One 13, 20 (2018).
Google Scholar 
15.Morris, P. A. A method for determining absolute age in the hedgehog. Notes Mammal Soc. 20, 277–280 (1970).
Google Scholar 
16.Castanet, et al. Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus. J. Zool. 263, 31–39 (2004).Article 

Google Scholar 
17.Klevezal, G. A. & Kleinenberg, S. E. Age determination of mammals by layered structures of teeth and bones. (1967).18.Barker, J. M., Boonstra, R. & Schulte-Hostedde, A. I. Age determination in yellow-pine chipmunks (Tamias amoenus): A comparison of eye lens masses and bone sections. Can. J. Zool. 81, 1774–1779 (2003).Article 

Google Scholar 
19.Amson, E., Kolb, C., Scheyer, T. M. & Sánchez-Villagra, M. R. Growth and life history of Middle Miocene deer (Mammalia, Cervidae) based on bone histology. C.R. Palevol 14, 637–645 (2015).Article 

Google Scholar 
20.Kolb, C. et al. Growth in fossil and extant deer and implications for body size and life history evolution. BMC Evol. Biol. 15, 19 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
21.de Buffrénil, V. & Pascal, M. Croissance et morphogénèse postnatales de la mandibule du vison (Mustela vison Schreiber): Données sur la dynamique et l’interprétation fonctionnelle des dépôts osseux mandibulaires. Can. J. Zool. 62, 2026–2037 (1984).Article 

Google Scholar 
22.Castanet, J., CurryRogers, K., Cubo, J. & Jacques-Boisard, J. Periosteal bone growth rates in extant ratites (ostriche and emu). Implications for assessing growth in dinosaurs. Comptes Rendus Acad. Sci. Ser. III Sci. Vie 323, 543–550 (2000).CAS 

Google Scholar 
23.Starck, J. M. & Chinsamy, A. Bone microstructure and developmental plasticity in birds and other dinosaurs. J. Morphol. 254, 232–246 (2002).PubMed 
Article 
PubMed Central 

Google Scholar 
24.de Margerie, E., Cubo, J. & Castanet, J. Bone typology and growth rate: Testing and quantifying ‘Amprino’s rule’ in the mallard (Anas platyrhynchos). Comptes Rendus Biol. 325, 221–230 (2002).Article 

Google Scholar 
25.de Margerie, E. et al. Assessing a relationship between bone microstructure and growth rate: A fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus). J. Exp. Biol. 207, 869–879 (2004).PubMed 
Article 
PubMed Central 

Google Scholar 
26.Montoya-Sanhueza, G., Bennett, N. C., Oosthuizen, M. K., Dengler-Crish, C. M. & Chinsamy, A. Bone remodeling in the longest living rodent, the naked mole-rat: Interelement variation and the effects of reproduction. J. Anat. https://doi.org/10.1111/joa.13404 (2021).Article 
PubMed 
PubMed Central 

Google Scholar 
27.Smith, T. M. Experimental determination of the periodicity of incremental features in enamel. J. Anat. 208, 99–113 (2006).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
28.Kierdorf, H., Kierdorf, U., Frölich, K. & Witzel, C. Lines of evidence-incremental markings in molar enamel of Soay sheep as revealed by a fluorochrome labeling and backscattered electron imaging study. PLoS One 8, 20 (2013).
Google Scholar 
29.Witzel, C., Kierdorf, U., Frölich, K. & Kierdorf, H. The pay-off of hypsodonty—timing and dynamics of crown growth and wear in molars of Soay sheep. BMC Evol. Biol. 18, 1–14 (2018).Article 

Google Scholar 
30.Kahle, P., Witzel, C., Kierdorf, U., Frölich, K. & Kierdorf, H. Mineral apposition rates in coronal dentine of mandibular first molars in Soay sheep: Results of a fluorochrome labeling study. Anat. Rec. 301, 902–912 (2018).CAS 
Article 

Google Scholar 
31.van Gaalen, S. M. et al. Use of fluorochrome labels in in vivo bone tissue engineering research. Tissue Eng. Part B. Rev. 16, 209–217 (2010).PubMed 
Article 
PubMed Central 

Google Scholar 
32.Shim, M.-J. Bone changes in femoral bone of mice using calcein labeling. Korean J. Clin. Lab. Sci. 48, 114–117 (2016).Article 

Google Scholar 
33.Klevezal, G. A. Recording Structures of Mammals (Balkema Publishers, 1996).34.Klevezal, G. A. & Mina, M. V. Tetracycline labelling as a method of field studies of individual growth and population structure in rodents. Lynx (Praha) 22, 67–78 (1984).
Google Scholar 
35.Smith, T. M., Reid, D. J. & Sirianni, J. E. The accuracy of histological assessments of dental development and age at death. J. Anat. 208, 125–138 (2006).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
36.Curtin, A. J. et al. Noninvasive histological comparison of bone growth patterns among fossil and extant neonatal elephantids using synchrotron radiation X-ray microtomography. J. Vertebr. Paleontol. 32, 939–955 (2012).Article 

Google Scholar 
37.Hugi, J. & Snchez-Villagra, M. R. Life history and skeletal adaptations in the galapagos marine iguana (Amblyrhynchus cristatus) as reconstructed with bone histological dataa comparative study of iguanines. J. Herpetol. 46, 312–324 (2012).Article 

Google Scholar 
38.Chinsamy, A. & Hurum, J. H. Bone microstructure and growth patterns of early mammals. Acta Palaeontol. Pol. 51, 325–338 (2006).
Google Scholar 
39.Teagasc. Development of the Calf Digestive System. Teagasc Calf Rearing Manual: Best Practice from Birth to Three Months 59–76 (2017).40.Warren, L. K., Lawrence, L. M., Parker, A. L., Barnes, T. & Griffin, A. S. The effect of weaning age on foal growth and radiographic bone density. J. Equine Vet. Sci. 18, 335–340 (1998).Article 

Google Scholar 
41.Holland, J. L. et al. Weaning stress is affected by nutrition and weaning methods. Pferdeheilkunde 12, 257–260 (1996).Article 

Google Scholar 
42.Enríquez, D., Hötzel, M. J. & Ungerfeld, R. Minimising the stress of weaning of beef calves: A review. Acta Vet. Scand. 53, 1–8 (2011).Article 

Google Scholar 
43.Pollard, J. C., Asher, G. W. & Littlejohn, R. P. Weaning date affects calf growth rates and hind conception dates in farmed red deer (Cervus elaphus). Anim. Sci. 74, 111–116 (2002).Article 

Google Scholar 
44.Wolter, B. F. & Ellis, M. The effects of weaning weight and rate of growth immediately after weaning on subsequent pig growth performance and carcass characteristics. Can. J. Anim. Sci. 81, 363–369 (2001).Article 

Google Scholar 
45.Pluske, J. R., Dividich, J. L. & Verstegen, M. W. A. Weaning the pig. Concepts and Consequences Weaning the Pig (Wageningen Academic Publishers, 2003). https://doi.org/10.3920/978-90-8686-513-0.46.Landete-Castillejos, T. et al. Milk production and composition in captive Iberian red deer (Cervus elaphus hispanicus): Effect of birth date. The online version of this article, along with updated information and services, is located on the World Wide Web at: Milk production. J. Anim. Sci. 78, 2771–2777 (2000).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
47.Wang, Y., Bekhit, A. E. D. A., Morton, J. D. & Mason, S. Nutritional value of deer milk. In Nutrients in Dairy and Their Implications for Health and Disease 363–375 (2017). https://doi.org/10.1016/B978-0-12-809762-5.00028-048.Stein, K. & Prondvai, E. Rethinking the nature of fibrolamellar bone: An integrative biological revision of sauropod plexiform bone formation. Biol. Rev. 89, 24–47 (2014).PubMed 
Article 
PubMed Central 

Google Scholar 
49.Clutton-Brock, T. H., Guiness, F. E. & Albon, S. D. Red Deer: Behaviour and Ecology of Two Sexes (The University of Chicago Press, 1982). https://doi.org/10.1016/0006-3207(83)90010-1.50.Festa-bianchet, M., Jorgenson, J. T. & Réale, D. Early development, adult mass, and reproductive success in bighorn sheep. Behav. Ecol. 11, 633–639 (2000).Article 

Google Scholar 
51.Cook, J. G. et al. Effects of summer–autumn nutrition and parturition date on reproduction and survival of elk. Wildl. Monogr. 20, 1–61 (2004).
Google Scholar 
52.Moore, G. H., Littlejohn, R. P. & Cowie, G. M. Liveweights, growth rates, and mortality of farmed red deer at Invermay. N. Z. J. Agric. Res. 31, 293–300 (1988).Article 

Google Scholar 
53.Ozanne, S. E. & Hales, C. N. Poor fetal growth followed by rapid postnatal catch-up growth leads to premature death. Mech. Ageing Dev. 126, 852–854 (2005).PubMed 
Article 
PubMed Central 

Google Scholar 
54.Van Eetvelde, M. & Opsomer, G. Innovative look at dairy heifer rearing: Effect of prenatal and post-natal environment on later performance. Reprod. Domest. Anim. 52, 30–36 (2017).PubMed 
Article 
PubMed Central 

Google Scholar 
55.Calderón, T., DeMiguel, D., Arnold, W., Stalder, G. & Köhler, M. Calibration of life history traits with epiphyseal closure, dental eruption and bone histology in captive and wild red deer. J. Anat. 20, 205–216. https://doi.org/10.1111/joa.13016 (2019).Article 

Google Scholar 
56.Horner, J. R., De Ricqlès, A. & Padian, K. Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: Growth dynamics and physiology based on an ontogenetic series of skeletal elements. J. Vertebr. Paleontol. 20, 115–129 (2000).Article 

Google Scholar 
57.Padian, K., De Ricqlès, A. J. & Horner, J. R. Dinosaurian growth rates and bird-origins. Nature 412, 405–408 (2001).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
58.Woodward, H. N., Padian, K. & Lee, A. H. Skeletochronology. In Bone Histology of Fossil Tetrapods (eds Padian, K. & Lamm, E.-T.) 195–216 (University of California Press, 2013).59.Pratt, I. V. & Cooper, D. M. L. The effect of growth rate on the three-dimensional orientation of vascular canals in the cortical bone of broiler chickens. J. Anat. 233, 531–541 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
60.Enlow, D. H. A study of the post-natal growth and remodelling of bone. Am. J. Anat. 110, 79–101 (1962).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
61.Chinsamy-Turan, A. The Microstructure of Dinosaur Bone (The Johns Hopkins University Press, 2005).62.de Buffrénil, V. & Quilhac, A. Bone tissue types: A brief account of currently used categories. in Vertebrate Skeletal Histology and Paleohistology (eds. de Buffrénil, V., de Riclès, J. A., Zylbeberg, L. & Padian, K.) 148–192 (CRC Press, 2021).63.Padian, K., Lamm, E.-T. & Werning, S. Selection of specimens. In Bone Histology of Fossil Tetrapods (eds Padian, K. & Lamm, E.-T.) 35–54 (University of California Press, 2013).64.Montoya-Sanhueza, G., Bennett, N. C., Oosthuizen, M. K., Dengler-Crish, C. M. & Chinsamy, A. Long bone histomorphogenesis of the naked mole-rat: Histodiversity and intraspecific variation. J. Anat. https://doi.org/10.1111/joa.13381 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
65.Calderón, T., DeMiguel, D., Arnold, W., Stalder, G. & Köhler, M. Calibration of life history traits with epiphyseal closure, dental eruption and bone histology in captive and wild red deer. J. Anat. https://doi.org/10.1111/joa.13016 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
66.Prondvai, E., Stein, K. H. W., de Ricqlès, A. & Cubo, J. Development-based revision of bone tissue classification: The importance of semantics for science. Biol. J. Linn. Soc. 112, 799–816 (2014).Article 

Google Scholar 
67.Francillon-Vieillot, H. et al. Microstructural and mineralization of vertebral skeletal tissues. In Skeletal Biommineralization: Patterns, Processes and Evolutionary Trends (ed. Carter, J. G.) (Van Nostrand Reinhold, 1990).68.Montes, L. et al. Relationships between bone growth rate, body mass and resting metabolic rate in growing amniotes: A phylogenetic approach. Biol. J. Linn. Soc. 92, 63–76 (2007).Article 

Google Scholar 
69.Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
70.Team, Rs. RStudio: Integrated Development for R. (2019).71.Muggeo, V. M. R. Interval estimation for the breakpoint in segmented regression: A smoothed score-based approach. Aust. N. Z. J. Stat. 59, 311–322 (2017).MathSciNet 
MATH 
Article 

Google Scholar  More

Centro de Investigação em Biodiversidade e Recursos Genéticos/Research Network in Biodiversity and Evolutionary Biology, Campus Agrário de Vairão, Universidade do Porto, Vairão, PortugalNuno Queiroz, Ana Couto, Marisa Vedor, Ivo da Costa, Gonzalo Mucientes & António M. SantosMarine Biological Association of the United Kingdom, Plymouth, UKNuno Queiroz, Nicolas E. Humphries, Lara L. Sousa, Samantha J. Simpson, Emily J. Southall & David W. SimsDepartamento de Biologia, Faculdade de Ciências da Universidade do Porto, Porto, PortugalMarisa Vedor & António M. SantosUWA Oceans Institute, Indian Ocean Marine Research Centre, University of Western Australia, Crawley, Western Australia, AustraliaAna M. M. SequeiraSchool of Biological Sciences, University of Western Australia, Crawley, Western Australia, AustraliaAna M. M. SequeiraSpanish Institute of Oceanography, Santa Cruz de Tenerife, SpainFrancisco J. AbascalAbercrombie and Fish, Port Jefferson Station, NY, USADebra L. AbercrombieMarine Biology and Aquaculture Unit, College of Science and Engineering, James Cook University, Cairns, Queensland, AustraliaKatya Abrantes, Adam Barnett, Richard Fitzpatrick & Marcus SheavesInstitute of Natural and Mathematical Sciences, Massey University, Palmerston North, New ZealandDavid Acuña-MarreroUniversidade Federal Rural de Pernambuco (UFRPE), Departamento de Pesca e Aquicultura, Recife, BrazilAndré S. Afonso, Natalia P. A. Bezerra, Fábio H. V. Hazin, Fernanda O. Lana, Bruno C. L. Macena & Paulo TravassosMARE, Marine and Environmental Sciences Centre, Instituto Politécnico de Leiria, Peniche, PortugalAndré S. AfonsoMARE, Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Cascais, PortugalPedro Afonso, Jorge Fontes & Frederic VandeperreInstitute of Marine Research (IMAR), Departamento de Oceanografia e Pescas, Universidade dos Açores, Horta, PortugalPedro Afonso, Jorge Fontes, Bruno C. L. Macena & Frederic VandeperreOkeanos – Departamento de Oceanografia e Pescas, Universidade dos Açores, Horta, PortugalPedro Afonso, Jorge Fontes & Frederic VandeperreDepartment of Environmental Affairs, Oceans and Coasts Research, Cape Town, South AfricaDarrell Anders, Michael A. Meÿer, Sarika Singh & Laurenne B. SnydersLarge Marine Vertebrates Research Institute Philippines, Jagna, PhilippinesGonzalo AraujoFins Attached Marine Research and Conservation, Colorado Springs, CO, USARandall ArauzPrograma Restauración de Tortugas Marinas PRETOMA, San José, Costa RicaRandall ArauzMigraMar, Olema, CA, USARandall Arauz, Sandra Bessudo Lion, Eduardo Espinoza, Alex R. Hearn, Mauricio Hoyos, James T. Ketchum, A. Peter Klimley, Cesar Peñaherrera-Palma, George Shillinger & German SolerInstitut de Recherche pour le Développement, UMR MARBEC (IRD, Ifremer, Univ. Montpellier, CNRS), Sète, FrancePascal Bach, Antonin V. Blaison, Laurent Dagorn, John D. Filmalter, Fabien Forget, Francois Poisson, Marc Soria & Mariana T. TolottiBiology Department, University of Massachusetts Dartmouth, Dartmouth, MA, USADiego Bernal & Heather MarshallRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaMichael L. Berumen, Jesse E. M. Cochran & Carlos M. DuarteFundación Malpelo y Otros Ecosistemas Marinos, Bogota, ColombiaSandra Bessudo Lion, Felipe Ladino, Lina Maria Quintero & German SolerHopkins Marine Station of Stanford University, Pacific Grove, CA, USABarbara A. Block, Taylor K. Chapple, George Shillinger & Timothy D. WhiteDepartment of Biological Sciences, Florida International University, North Miami, FL, USAMark E. Bond, Demian D. Chapman & Yannis P. PapastamatiouInstituto de Ciências do Mar, Universidade Federal do Ceará, Fortaleza, BrazilRamon BonfilCSIRO Oceans and Atmosphere, Hobart, Tasmania, AustraliaRussell W. Bradford & Barry D. BruceSchool of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USACamrin D. BraunBiology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USACamrin D. Braun & Simon R. ThorroldShark Research and Conservation Program, Cape Eleuthera Institute, Eleuthera, BahamasEdward J. Brooks, Annabelle Brooks & Sean WilliamsUniversity of Exeter, Exeter, UKAnnabelle BrooksSouth Atlantic Environmental Research Institute, Stanley, Falkland IslandsJudith BrownDepartment of Biological Sciences, The Guy Harvey Research Institute, Nova Southeastern University, Dania Beach, FL, USAMichael E. Byrne, Mahmood Shivji, Jeremy J. Vaudo & Bradley M. WetherbeeSchool of Natural Resources, University of Missouri, Columbia, MO, USAMichael E. ByrneLife and Environmental Sciences, University of Iceland, Reykjavik, IcelandSteven E. CampanaSchool of Marine Science and Policy, University of Delaware, Lewes, DE, USAAaron B. Carlisle & Gregory B. SkomalMassachusetts Division of Marine Fisheries, New Bedford, MA, USAJohn ChisholmMarine Research Facility, Jeddah, Saudi ArabiaChristopher R. Clarke & James S. E. LeaPSL, Labex CORAIL, CRIOBE USR3278 EPHE-CNRS-UPVD, Papetoai, French PolynesiaEric G. CluaAgence de Recherche pour la Biodiversité à la Réunion (ARBRE), Réunion, Marseille, FranceEstelle C. CrocheletInstitut de Recherche pour le Développement, UMR 228 ESPACE-DEV, Réunion, Marseille, FranceEstelle C. CrocheletSave Our Seas Foundation–D’Arros Research Centre (SOSF-DRC), Geneva, SwitzerlandRyan Daly & Clare A. Keating DalySouth African Institute for Aquatic Biodiversity (SAIAB), Grahamstown, South AfricaRyan Daly, John D. Filmalter, Enrico Gennari & Alison A. KockDepartment of Fisheries Evaluation, Fisheries Research Division, Instituto de Fomento Pesquero (IFOP), Valparaíso, ChileDaniel Devia CortésSchool of Biological, Earth and Environmental Sciences, University College Cork, Cork, IrelandThomas K. Doyle & Luke HarmanMaREI Centre, Environmental Research Institute, University College Cork, Cork, IrelandThomas K. DoyleCollege of Science and Engineering, Flinders University, Adelaide, South Australia, AustraliaMichael Drew, Matthew Heard & Charlie HuveneersDepartment of Conservation, Auckland, New ZealandClinton A. J. DuffySouth African Institute for Aquatic Biodiversity, Geological Sciences, UKZN, Durban, South AfricaThor EriksonDireccion Parque Nacional Galapagos, Puerto Ayora, Galapagos, EcuadorEduardo EspinozaAustralian Institute of Marine Science, Indian Ocean Marine Research Centre (UWA), Crawley, Western Australia, AustraliaLuciana C. Ferreira, Mark G. Meekan & Michele ThumsDepartment of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, VA, USAFrancesco FerrettiOCEARCH, Park City, UT, USAG. Chris FischerBedford Institute of Oceanography, Dartmouth, Nova Scotia, CanadaMark Fowler, Warren Joyce & Anna MacDonnellNational Institute of Water and Atmospheric Research, Wellington, New ZealandMalcolm P. Francis & Warrick S. LyonBeneath the Waves, Herndon, VA, USAAustin J. GallagherRosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, USAAustin J. Gallagher, Neil Hammerschlag & Emily R. NelsonOceans Research Institute, Mossel Bay, South AfricaEnrico GennariDepartment of Ichthyology and Fisheries Science, Rhodes University, Grahamstown, South AfricaEnrico Gennari & Alison TownerSARDI Aquatic Sciences, Adelaide, South Australia, AustraliaSimon D. Goldsworthy & Paul J. RogersZoological Society of London, London, UKMatthew J. Gollock & Fiona LlewellynGalapagos Whale Shark Project, Puerto Ayora, Galapagos, EcuadorJonathan R. GreenGriffith Centre for Coastal Management, Griffith University School of Engineering, Griffith University, Gold Coast, Queensland, AustraliaJohan A. GustafsonSaving the Blue, Cooper City, FL, USATristan L. GuttridgeSmithsonian Tropical Research Institute, Panama City, PanamaHector M. GuzmanLeonard and Jayne Abess Center for Ecosystem Science and Policy, University of Miami, Coral Gables, FL, USANeil HammerschlagGalapagos Science Center, San Cristobal, Galapagos, EcuadorAlex R. HearnUniversidad San Francisco de Quito, Quito, EcuadorAlex R. HearnBlue Water Marine Research, Tutukaka, New ZealandJohn C. HoldsworthUniversity of Queensland, Brisbane, Queensland, AustraliaBonnie J. HolmesMicrowave Telemetry, Columbia, MD, USALucy A. Howey & Lance K. B. JordanPelagios-Kakunja, La Paz, MexicoMauricio Hoyos & James T. KetchumMote Marine Laboratory, Center for Shark Research, Sarasota, FL, USARobert E. Hueter, John J. Morris & John P. TyminskiBiological Sciences, University of Windsor, Windsor, Ontario, CanadaNigel E. HusseyCape Research and Diver Development, Simon’s Town, South AfricaDylan T. IrionInstitute of Zoology, Zoological Society of London, London, UKDavid M. P. JacobyCentre for Sustainable Aquatic Ecosystems, Harry Butler Institute, Murdoch University, Perth, Western Australia, AustraliaOliver J. D. JewellDyer Island Conservation Trust, Western Cape, South AfricaOliver J. D. Jewell & Alison TownerBlue Wilderness Research Unit, Scottburgh, South AfricaRyan JohnsonUniversity of California Davis, Davis, CA, USAA. Peter KlimleyCape Research Centre, South African National Parks, Steenberg, South AfricaAlison A. KockShark Spotters, Fish Hoek, South AfricaAlison A. KockInstitute for Communities and Wildlife in Africa, Department of Biological Sciences, University of Cape Town, Rondebosch, South AfricaAlison A. KockWestern Cape Department of Agriculture, Veterinary Services, Elsenburg, South AfricaPieter KoenDepartamento de Biologia Marinha, Universidade Federal Fluminense (UFF), Niterói, BrazilFernanda O. LanaDepartment of Zoology, University of Cambridge, Cambridge, UKJames S. E. LeaAtlantic White Shark Conservancy, Chatham, MA, USAHeather MarshallFisheries and Aquaculture Centre, Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, AustraliaJaime D. McAllister, Jayson M. Semmens, German Soler & Kilian M. StehfestPontificia Universidad Católica del Ecuador Sede Manabi, Portoviejo, EcuadorCesar Peñaherrera-PalmaMarine Megafauna Foundation, Truckee, CA, USASimon J. Pierce & Christoph A. RohnerConservation and Fisheries Department, Ascension Island Government, Georgetown, Ascension Island, UKAndrew J. RichardsonMarine Conservation Society Seychelles, Victoria, SeychellesDavid R. L. RowatCORDIO, East Africa, Mombasa, KenyaMelita SamoilysUpwell, Monterey, CA, USAGeorge ShillingerDepartment of Zoology and Institute for Coastal and Marine Research, Nelson Mandela University, Port Elizabeth, South AfricaMalcolm J. SmaleNational Institute of Polar Research, Tachikawa, Tokyo, JapanYuuki Y. WatanabeSOKENDAI (The Graduate University for Advanced Studies), Tachikawa, Tokyo, JapanYuuki Y. WatanabeCentre for Ecology and Conservation, University of Exeter, Penryn, UKSam B. WeberDepartment of Biological Sciences, University of Rhode Island, Kingston, RI, USABradley M. WetherbeeDepartment of Oceanography and Environment, Fisheries Research Division, Instituto de Fomento Pesquero (IFOP), Valparaíso, ChilePatricia M. ZárateDepartment of Biological Sciences, Macquarie University, Sydney, New South Wales, AustraliaRobert HarcourtSchool of Life and Environmental Sciences, Deakin University, Geelong, Victoria, AustraliaGraeme C. HaysAZTI – BRTA, Pasaia, SpainXabier IrigoienIKERBASQUE, Basque Foundation for Science, Bilbao, SpainXabier IrigoienInstituto de Fisica Interdisciplinar y Sistemas Complejos, Consejo Superior de Investigaciones Cientificas, University of the Balearic Islands, Palma de Mallorca, SpainVictor M. EguiluzWildlife Conservation Research Unit, Department of Zoology, University of Oxford, Tubney, UKLara L. SousaOcean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton, UKSamantha J. Simpson & David W. SimsCentre for Biological Sciences, University of Southampton, Southampton, UKDavid W. SimsN.Q. and D.W.S. planned the data analysis. N.Q. led the data analysis with contributions from M.V., A.M.M.S. and D.W.S. N.E.H. contributed analysis tools. A.M.M.S. undertook linear-regression modelling. D.W.S. led the manuscript writing with contributions from N.Q., N.E.H., A.M.M.S and all authors. Six of the original authors were not included in the Reply authorship; two authors retired from science and the remaining four, although supportive of our Reply, declined to join the authorship due to potential conflicts of interest with the authors of the Comment and/or their institutions. More

Study areaThe Pearl River Delta (112°45′–113°50′ E, 21°31′–23°10′ N) is located in the central and southern parts of Guangdong Province, including the lower reaches of the Pearl River, adjacent to Hong Kong and Macao, and facing Southeast Asia across the sea with convenient land and sea transportation. As shown in Fig. 1, the Pearl River Delta region includes nine prefecture-level cities, namely Guangzhou, Shenzhen, Zhongshan, Zhuhai, Dongguan, Zhaoqing, Foshan, Huizhou, and Jiangmen.Figure 1Geographical location of Pearl River Delta drawn in ArcGIS 10.6.Full size imageData sourceThe research framework of this paper is shown in Fig. 2, and the data sources are as follows. Taking the basin as the research unit, the raster data of 30 m and 1 km were analyzed by zoning statistics:

(1)

China’s land-use raster data for 1990, 2000, 2010, and 2018 were obtained from the Data Center for Resources and Environmental Sciences, Chinese Academy of Sciences (http://www.resdc.cn), with a spatial resolution of 30 m. According to land resources and their utilization attributes, the dataset divides land cover types into six first-level categories: cultivated land, woodland, grassland, water area, construction land, unused land, and land reclamation from ocean. The land urbanization rate (LUR) refers to the proportion of construction land in the whole region, which is calculated by dividing the area of construction land by the area of all land use types.

(2)

Raster data of population density (POP) from 1990, 2000, 2010, and 2015 were obtained from the Environment and Resources Data Cloud Platform of the Chinese Academy of Sciences, with a spatial resolution of 1 km. Owing to the stable growth of population density under normal circumstances, the population density data of 2018 were obtained by linear fitting based on POP data from 2010 and 2015.

(3)

Nighttime Light (NTL) raster data from 1992 to 2018 were obtained from the Nature journal data (https://doi.org/10.6084/m9.figshare.9828827.v2) with a spatial resolution of 500 m45 Calibration was performed to eliminate the differences in the DMSP (1992–2013) and VIIRS (2012–2018) data, generating a complete and consistent NTL dataset on a global scale.

Figure 2Research framework.Full size imageLand-use information TUPUThe land-use information graph is a geospatial analysis model combining attributes, processes, and spaces, which can reflect the spatial differences and temporal changes in land-use types46. In its function expression, let the state variables be (pleft( {p_{1} ,p_{2} ,p_{3} , ldots ,p_{n} } right)), and then set p as a function of spatial position r and time t, as follows:$$ begin{array}{*{20}c} {p = fleft( {r,t} right)} \ end{array} $$
(1)
where (p) represents land-use characteristics. (1) To realize the spatial description of land attributes, when t is constant, the function relation of (p) changing with (r) is constructed. (2) The process description of land attributes can be realized, and when (r) is constant, the function relation of (p) changing with (t) can be constructed. The combination of these two functions can form a conceptual model of the land-use information graph and realize a composite study of land space, process, and attributes.Habitat qualityHabitat quality evaluationWe used InVEST-HQ to evaluate the habitat quality in the Pearl River Delta region. Based on land-use types, InVEST-HQ calculated the habitat degradation degree and habitat quality index by using threat factors, the sensitivity of different habitat types to threat factors, and habitat suitability15. The InVEST-HQ model was co-developed by Stanford University, the Nature Conservancy, and the World Wide Fund for Nature15. InVEST-HQ has a low demand for data and a better spatial visualization effect, which is widely used in the field of urban ecology47,48,49. For example, The InVEST-HQ model has been used to assess dynamic changes in habitat quality in Scottish11, China50,51 and Portugal47. Habitat degradation and habitat quality were calculated using the following formulas:$$ begin{array}{*{20}c} {Q_{{xj}} = ~H_{j} left[ {1 – left( {frac{{D_{{xj}}^{2} }}{{D_{{xj}}^{2} + k^{2} )}}} right)} right]} \ end{array} $$
(2)
$$ begin{array}{*{20}c} {D_{{xj}} = ~mathop sum limits_{{r = 1}}^{r} mathop sum limits_{{y = 1}}^{y} left( {frac{{w_{r} }}{{mathop sum nolimits_{{r = 1}}^{r} w_{r} }}} right)r_{y} i_{{rxy}} beta _{x} S_{{jr}} } \ end{array} $$
(3)
where (Q_{{xj}}) is the habitat quality of grid x in land-use type j, (H_{j}) is the habitat suitability of land-use type j, (D_{{xj}}) is the habitat degradation degree of grid x in land-use type j, k is the half-satiety sum constant, r is the number of threat factors, and y is the relative sensitivity of threat sources. (r_{y} ,w_{r}), and (i_{{rxy}}) are, respectively, the interference intensity and weight of the grid where the threat factor r is located, and the interference generated by the habitat. (beta _{x} ,S_{{jr}}) are the anti-disturbance ability of habitat type x and its relative sensitivity to various threat sources, respectively.The value range of habitat degradation degree is [0, 1], and the larger the value, the more serious the habitat degradation. The value of habitat quality is between 0 and 1, and the higher the value, the better the habitat quality.$$ begin{array}{*{20}c} {Linear,attenuation:~i_{{rxy}} = 1 – left( {d_{{xy}} /d_{{r,max}} } right)} \ end{array} $$
(4)
$$ begin{array}{*{20}c} {Exponential,decay:~i_{{rxy}} = expleft[ { – 2.99d_{{xy}} /d_{{r{text{~}}max}} } right]} \ end{array} $$
(5)

where (d_{{xy}}) is the straight-line distance between grids x and y, and (d_{{r,max}}) is the maximum threat distance of threat factor r.Five categories of documentation are prepared before using InVEST-HQ: LULC maps, threat factor data, threat sources, accessibility of degradation sources, habitat types and their sensitivity to each threat. Threat sources were divided into Cropland, City/town, Rural settlements, Other construction land, Unused land, and land applications. The maps of threat sources are generated in ArcGIS. For example, in the map of threat sources of cultivated land, the raster value of cultivated land is set to 1, and the raster value of other land types is set to 0. Distance between habitats and threat sources, weight of threat factors, decay type of threats factors, habitat suitability and the sensitivity of different habitat types to threat factors were derived from previous studies in similar regions2,25,38,39,50 and user guide manual of InVEST model15, as shown in Tables 1 and 2.Table 1 Threat factors and related coefficients.Full size tableTable 2  Sensitivity of habitat types to each threat factor.Full size tableHabitat quality change index and contribution indexThe CI was used to analyze the causes of the changes in habitat quality, and the following formula was used to qu2,25,38,39,50antitatively represent the contribution of land-use conversion to habitat quality change. In this study, the total value of habitat quality loss caused by land transfer in areas related to construction land expansion from 1990 to 2018 can be expressed as follows:$$ begin{array}{*{20}c} {CI~ = ~frac{{mathop sum nolimits_{1}^{n} left( {Q_{{ij2018}} – Q_{{xj1990}} } right)}}{n}} \ end{array} $$
(6)

where n is the grid number of cultivated land transferred to construction land.To analyze the relationship between land-use change and habitat quality, the HQCI was constructed to describe the mean value of habitat quality reduction caused by land transfer in the areas related to construction land expansion during the study period. The formula is as follows:$$ begin{array}{*{20}c} {HQCI~ = CI_{{ij}} /S_{{ij}} } \ end{array} $$
(7)
where (CI_{{ij}}) represents the total value of habitat quality change when land-use type (i) is converted into land-use type (j), and (S_{{ij}}) represents the area converted from land-use type (i) into land-use type (j). The positive and negative values of HQCI, respectively, represent the positive and negative impacts of land-use change on the habitat, and the higher the absolute value of HQCI, the greater the impact.Correlation analysisGeographically weighted regressionBased on traditional OLS, GWR establishes local spatial regression and considers spatial location factors, which can effectively analyze the spatial heterogeneity of various elements at different locations52. The calculation formula is as follows:$$ Y_{i} = ~beta _{0} left( {mu _{i} ,v_{i} } right) + sum kbeta _{k} left( {mu _{i} ,v_{i} } right)X_{{ik}} + varepsilon _{i} $$where (Y_{i}) is the coupling coordination degree of the ith sample point, (left( {mu _{i} ,v_{i} } right)) is the spatial position coordinate of the ith sample point, (beta _{k} left( {mu _{i} ,v_{i} } right)) is the value of the continuous function (beta _{k} left( {mu ,v} right)) at (left( {mu _{i} ,v_{i} } right)), (X_{{ik}}) is the independent variable, (varepsilon _{i}) is the random error term, and k is the number of spatial units.To simplify the complicated urbanization process, it was divided into three aspects: economic urbanization, population urbanization, and land urbanization according to the existing research38. The NTL, POP, and LUR were used to represent the economic development, population scale, and land urbanization level of the city.The research unit is a river basin, which has both natural and social attributes. It is a relatively independent and complete system, which can connect and explain the coupling phenomenon of society, economy, and nature53. The hydrological analysis module in ArcGIS was used to divide the research area into 374 small basins. When calculating the cumulative flow of the grid, 100,000 was used as the threshold value, and basins less than 5 km2 were combined with the adjacent basins.Zone classification using the Self-organizing feature mapping neural networkThe SOFM neural network was proposed by Kohonen, a Finnish scholar, and constructed by simulating a “lateral inhibition” phenomenon in the human cerebral cortex. It has been widely applied in classification research in geographic and land system science42,43. The advantages of the SOFM neural network in classifying the coupling relationship between urbanization and habitat quality are as follows : (1) it simulates human brain neurons through unsupervised learning, which is objective and reliable. (2) It maintains the data topology during self-learning, training, and simulation to obtain reasonable partition results and identify the differences between different basins. (3) For massive data, the SOFM network has a good clustering function while maintaining its characteristics and uses the weight vector of the output node to represent the original input. The SOFM neural network can compress the data while maintaining a high similarity between the compression results and the original input data54. We exported the data from ArcGIS, and conducted cluster analysis on the four factors of NTL, POP, LUR and habitat quality using SOFM. Finally, the analysis results are imported into ArcGIS for display. More

An umbrella-shaped structure of unknown function crowns a recently described species of fairy lantern. Credit: Siti Munirah Mat Yunoh et al./PhytoKeys (CC BY 4.0)

Conservation biology
07 July 2021
Newfound ‘fairy lantern’ could soon be snuffed out forever

Wild boars have destroyed three of the four known specimens of a bizarre plant in the forests of Malaysia.

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Researchers have discovered a new species of ‘fairy lantern’, leafless plants that look like tiny glowing lights. Sadly, however, the organism might already be on the verge of extinction.Plants in the genus Thismia, colloquially called ‘fairy lanterns’, draw nutrients from underground fungi and grow in parts of Asia, Australasia and the Americas. Siti Munirah Mat Yunoh at the Forest Research Institute Malaysia in Kepong and her colleagues described a new species of Thismia that was first found in 2019 in a Malaysian rain forest. The scientists named the plant Thismia sitimeriamiae after the mother of the local explorer who discovered it, in honour of her support for her son’s nature-conservation efforts.Thismia sitimeriamiae is only about two centimetres tall, and sports an orange flower shaped like a funnel with an umbrella-like structure on top. The plant seems to be so rare that it should be considered critically endangered: just four individuals of T. sitimeriamiae have ever been seen, and wild boars have destroyed all but one of these, the authors say.

PhytoKeys (2021)

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1.Gaston, K. J., Bennie, J., Davies, T. W. & Hopkins, J. The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biol. Rev. 88, 912–927 (2013).PubMed 
Article 
PubMed Central 

Google Scholar 
2.Gaston, K. J., Davies, T. W., Nedelec, S. L. & Holt, L. A. Impacts of artificial light at night on biological timings. Annu. Rev. Ecol. Evol. Syst. 48, 49–68 (2017).Article 

Google Scholar 
3.Falchi, F. et al. The new world atlas of artificial night sky brightness. Sci. Adv. 2, e1600377 (2016).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
4.Kyba, C. C. et al. Artificially lit surface of Earth at night increasing in radiance and extent. Sci. Adv. 3, e1701528 (2017).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
5.Gaston, K. J., Gaston, S., Bennie, J. & Hopkins, J. Benefits and costs of artificial nighttime lighting of the environment. Environ. Rev. 23, 14–23 (2014).Article 

Google Scholar 
6.Sanders, D., Frago, E., Kehoe, R., Patterson, C. & Gaston, K. J. A meta-analysis of biological impacts of artificial light at night. Nat. Ecol. Evol. 5, 74–81 (2020).PubMed 
Article 
PubMed Central 

Google Scholar 
7.Dominoni, D., Quetting, M. & Partecke, J. Artificial light at night advances avian reproductive physiology. Proc. R. Soc. B Biol. Sci. 280, 20123017 (2013).Article 
CAS 

Google Scholar 
8.Owens, A. C. S. & Lewis, S. M. The impact of artificial light at night on nocturnal insects: a review and synthesis. Ecol. Evol. 8, 11337–11358 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
9.Becker, A., Whitfield, A. K., Cowley, P. D., Järnegren, J. & Næsje, T. F. Potential effects of artificial light associated with anthropogenic infrastructure on the abundance and foraging behaviour of estuary-associated fishes. J. Appl. Ecol. 50, 43–50 (2013).Article 

Google Scholar 
10.van Grunsven, R. H. A. et al. Experimental light at night has a negative long-term impact on macro-moth populations. Curr. Biol. 30, R694–R695 (2020).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
11.Macgregor, C. J., Evans, D. M., Fox, R. & Pocock, M. J. O. The dark side of street lighting: impacts on moths and evidence for the disruption of nocturnal pollen transport. Glob. Change Biol. 23, 697–707 (2017).ADS 
Article 

Google Scholar 
12.Knop, E. et al. Artificial light at night as a new threat to pollination. Nature 548, 206–209 (2017).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
13.Lewis, S. M. et al. A global perspective on firefly extinction threats. BioScience 70, 157–167 (2020).Article 

Google Scholar 
14.Johnsen, S. et al. Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. J. Exp. Biol. 209, 789–800 (2006).PubMed 
Article 
PubMed Central 

Google Scholar 
15.Macgregor, C. J., Pocock, M. J. O., Fox, R. & Evans, D. M. Effects of street lighting technologies on the success and quality of pollination in a nocturnally pollinated plant. Ecosphere 10, e02550 (2019).Article 

Google Scholar 
16.Troscianko, J., Wilson-Aggarwal, J., Stevens, M. & Spottiswoode, C. N. Camouflage predicts survival in ground-nesting birds. Sci. Rep. 6, 19966 (2016).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
17.Endler, J. A. Signals, signal conditions, and the direction of evolution. Am. Nat. S125–S153 (1992).18.Davies, T. W., Bennie, J., Inger, R., de Ibarra, N. H. & Gaston, K. J. Artificial light pollution: are shifting spectral signatures changing the balance of species interactions? Glob. Change Biol. 19, 1417–1423 (2013).ADS 
Article 

Google Scholar 
19.Lamphar, H. A. S. & Kocifaj, M. Light pollution in ultraviolet and visible spectrum: effect on different visual perceptions. PLoS ONE 8, e56563 (2013).ADS 
Article 
CAS 

Google Scholar 
20.Longcore, T. et al. Rapid assessment of lamp spectrum to quantify ecological effects of light at night. J. Exp. Zool. A Ecol. Integr. Physiol. 329, 511–521 (2018).PubMed 
Article 
PubMed Central 

Google Scholar 
21.Seymoure, B. M., Linares, C. & White, J. Connecting spectral radiometry of anthropogenic light sources to the visual ecology of organisms. J. Zool. 308, 93–110 (2019).Article 

Google Scholar 
22.Vorobyev, M. & Osorio, D. Receptor noise as a determinant of colour thresholds. Proc. R. Soc. Lond. B Biol. Sci. 265, 351–358 (1998).CAS 
Article 

Google Scholar 
23.Kelber, A., Yovanovich, C. & Olsson, P. Thresholds and noise limitations of colour vision in dim light. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160065 (2017).Article 

Google Scholar 
24.Olsson, P., Lind, O. & Kelber, A. Bird colour vision: behavioural thresholds reveal receptor noise. J. Exp. Biol. 218, 184–193 (2015).PubMed 
Article 
PubMed Central 

Google Scholar 
25.Walton, R. E., Sayer, C. D., Bennion, H. & Axmacher, J. C. Nocturnal pollinators strongly contribute to pollen transport of wild flowers in an agricultural landscape. Biol. Lett. 16, 20190877 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
26.Kelber, A., Balkenius, A. & Warrant, E. J. Scotopic colour vision in nocturnal hawkmoths. Nature 419, 922–925 (2002).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
27.Renoult, J. P., Kelber, A. & Schaefer, H. M. Colour spaces in ecology and evolutionary biology. Biol. Rev. 92, 292–315 (2017).PubMed 
Article 
PubMed Central 

Google Scholar 
28.Cook, L. M., Grant, B. S., Saccheri, I. J. & Mallet, J. Selective bird predation on the peppered moth: the last experiment of Michael Majerus. Biol. Lett. 8, 609–612 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
29.Svensson, M. G. E., Rydell, J. & Töve, J. Deep flowers for long tongues. Trends Ecol. Evol. 13, 460 (1998).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
30.Dominoni, D. M. The effects of light pollution on biological rhythms of birds: an integrated, mechanistic perspective. J. Ornithol. 156, 409–418 (2015).Article 

Google Scholar 
31.Russ, A., Rüger, A. & Klenke, R. Seize the night: European Blackbirds (Turdus merula) extend their foraging activity under artificial illumination. J. Ornithol. 156, 123–131 (2015).Article 

Google Scholar 
32.Hart, N. S., Partridge, J. C., Cuthill, I. C. & Bennett, A. T. Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). J. Comp. Physiol. A 186, 375–387 (2000).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
33.Wink, M. & Theile, V. Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera: Sphingidae). Chemoecology 12, 29–46 (2002).CAS 
Article 

Google Scholar 
34.Hundsdoerfer, A. K., Tshibangu, J. N., Wetterauer, B. & Wink, M. Sequestration of phorbol esters by aposematic larvae of Hyles euphorbiae (Lepidoptera: Sphingidae)? Chemoecology 15, 261–267 (2005).CAS 
Article 

Google Scholar 
35.Petschenka, G. & Dobler, S. Target-site sensitivity in a specialized herbivore towards major toxic compounds of its host plant: the Na+ K+-ATPase of the oleander hawk moth (Daphnisnerii) is highly susceptible to cardenolides. Chemoecology 19, 235 (2009).CAS 
Article 

Google Scholar 
36.Vallin, A., Jakobsson, S. & Wiklund, C. “An eye for an eye”?—on the generality of the intimidating quality of eyespots in a butterfly and a hawkmoth. Behav. Ecol. Sociobiol. 61, 1419–1424 (2007).Article 

Google Scholar 
37.Barber, J. R. & Kawahara, A. Y. Hawkmoths produce anti-bat ultrasound. Biol. Lett. 9, 20130161 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
38.Stevens, M., Troscianko, J., Wilson-Aggarwal, J. K. & Spottiswoode, C. N. Improvement of individual camouflage through background choice in ground-nesting birds. Nat. Ecol. Evol. 1, 1325 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
39.Kang, C., Moon, J.-Y., Lee, S.-I. & Jablonski, P. G. Moths use multimodal sensory information to adopt adaptive resting orientations. Biol. J. Linn. Soc. 111, 900–904 (2014).Article 

Google Scholar 
40.Kang, C., Stevens, M., Moon, J., Lee, S.-I. & Jablonski, P. G. Camouflage through behavior in moths: the role of background matching and disruptive coloration. Behav. Ecol. 26, 45–54 (2014).Article 

Google Scholar 
41.Falchi, F., Cinzano, P., Elvidge, C. D., Keith, D. M. & Haim, A. Limiting the impact of light pollution on human health, environment and stellar visibility. J. Environ. Manag. 92, 2714–2722 (2011).CAS 
Article 

Google Scholar 
42.Gaston, K. J., Davies, T. W., Bennie, J. & Hopkins, J. Reducing the ecological consequences of night-time light pollution: options and developments. J. Appl. Ecol. 49, 1256–1266 (2012).PubMed 
PubMed Central 
Article 

Google Scholar 
43.Longcore, T. et al. Tuning the White Light Spectrum of Light Emitting Diode Lamps to Reduce Attraction of Nocturnal Arthropods. Phil. Trans. B 370 (1667): 20140125 (2015).44.van Langevelde, F., Ettema, J. A., Donners, M., WallisDeVries, M. F. & Groenendijk, D. Effect of spectral composition of artificial light on the attraction of moths. Biol. Conserv. 144, 2274–2281 (2011).Article 

Google Scholar 
45.Somers-Yeates, R., Hodgson, D., McGregor, P. K., Spalding, A. & Ffrench-Constant, R. H. Shedding light on moths: shorter wavelengths attract noctuids more than geometrids. Biol. Lett. 9, 20130376 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
46.Donners, M. et al. Colors of attraction: modeling insect flight to light behavior. J. Exp. Zoo. A 329, 434–440 (2018).Article 

Google Scholar 
47.Jones, T. M., Durrant, J., Michaelides, E. B. & Green, M. P. Melatonin: a possible link between the presence of artificial light at night and reductions in biological fitness. Philos. Trans. R. Soc. Lond. B 370, 20140122 (2015).Article 
CAS 

Google Scholar 
48.Arnold, S. E., Faruq, S., Savolainen, V., McOwan, P. W. & Chittka, L. FReD: the floral reflectance database—a web portal for analyses of flower colour. PLoS ONE 5, e14287 (2010).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
49.Troscianko, J. & Stevens, M. Image calibration and analysis toolbox – a free software suite for objectively measuring reflectance, colour and pattern. Methods Ecol. Evol. 6, 1320–1331 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
50.R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2013).51.Gomez, D. et al. The intensity threshold of colour vision in a passerine bird, the blue tit (Cyanistes caeruleus). J. Exp. Biol. 217, 3775–3778 (2014).PubMed 
PubMed Central 

Google Scholar 
52.Bates, D., Maechler, M., Bolker, B. & Walker, S. lme4: Linear mixed-effects models using Eigen and S4. (2014).53.Maia, R. & White, T. E. Comparing colors using visual models. Behav. Ecol. 29, 649–659 (2018).Article 

Google Scholar 
54.Maia, R., Gruson, H., Endler, J. A. & White, T. E. pavo 2: New tools for the spectral and spatial analysis of colour in r. Methods Ecol. Evol. 10, 1097–1107 (2019).Article 

Google Scholar  More

1.Baker, P. J., Newman, T. & Harris, S. Bristol’s foxes—40 years of change. Br. Wildl. 12, 411–417 (2001).
Google Scholar 
2.Vuorisalo, T. et al. Urban development from an avian perspective: Causes of hooded crow (Corvus corone cornix) urbanization in two Finnish cities. Landsc. Urban Plan. 62, 69–87 (2003).Article 

Google Scholar 
3.Baker, P. J. & Harris, S. Urban mammals: What does the future hold? An analysis of the factors affecting patterns of use of residential gardens in Great Britain. Mammal Rev. 37, 297–315 (2007).
Google Scholar 
4.Evans, K. L., Hatchwell, B. J., Parnell, M. & Gaston, K. J. A conceptual framework for the colonization of urban areas: The blackbird Turdus merula as a case study. Biol. Rev. 85, 643–667 (2010).PubMed 

Google Scholar 
5.Geiger, M., Taucher, A. L., Gloor, S., Hegglin, D. & Bontadina, F. In the footsteps of city foxes: Evidence for a rise of urban badger populations in Switzerland. Hystrix It. J. Mamm. 29, 236–238 (2018).
Google Scholar 
6.Lesiński, G., Gryz, J., Krauze-Gryz, D. & Stolarz, P. Population increase and synurbization of the yellow-necked mouse Apodemus flavicollis in some wooded areas of Warsaw agglomeration, Poland, in the years 1983–2018. Urban Ecosyst. 24, 481–489 (2021).Article 

Google Scholar 
7.Andrzejewski, R., Babińska-Werka, J., Gliwicz, J. & Goszczyński, J. Synurbization processes in population of Apodemus agrarius. I. Characteristics of populations in an urbanization gradient. Acta Theriol. 23, 341–358 (1978).Article 

Google Scholar 
8.Doncaster, C. P. & MacDonald, D. W. Drifting territoriality in the red fox Vulpes vulpes. J. Anim. Ecol. 60, 423–439 (1991).Article 

Google Scholar 
9.Baker, P. J., Ansell, R. J., Dodds, P. A. A., Webber, C. E. & Harris, S. Factors affecting the distribution of small mammals in urban areas. Mammal Rev. 33, 95–100 (2003).Article 

Google Scholar 
10.Baker, P. J., Dowding, C. V., Molony, S. E., White, P. C. L. & Harris, S. Activity patterns of urban red foxes (Vulpes vulpes) reduce the risk of traffic-induced mortality. Behav. Ecol. 35, 716–724 (2007).Article 

Google Scholar 
11.Bateman, P. W. & Fleming, P. A. Big city life: Carnivores in urban environments. J. Zool. 287, 1–23 (2012).Article 

Google Scholar 
12.Harris, S. Distribution, habitat utilisation and age structure of a suburban fox (Vulpes vulpes) population. Mammal Rev. 7, 25–39 (1977).Article 

Google Scholar 
13.Harris, S. & Rayner, J. M. V. Urban fox (Vulpes vulpes) population estimates and habitat requirements in several British cities. J. Anim. Ecol. 55, 575–591 (1986).Article 

Google Scholar 
14.Adkins, C. A. & Stott, P. Home ranges, movements and habitat associations of red foxes Vulpes vulpes in suburban Toronto, Ontario, Canada. J. Zool. 244, 335–346 (1998).Article 

Google Scholar 
15.Duduś, L., Zalewski, A., Kozioł, O., Jakubiec, Z. & Król, N. Habitat selection by two predators in an urban area: The stone marten and red fox in Wrocław (SW Poland). Mamm. Biol. 79, 71–76 (2014).Article 

Google Scholar 
16.Harris, S. The food of suburban foxes (Vulpes vulpes) with special reference to London. Mammal Rev. 11, 151–168 (1981).Article 

Google Scholar 
17.Doncaster, C. P., Dickman, C. R. & MacDonald, D. W. Feeding ecology of red foxes (Vulpes vulpes) in the city of Oxford, England. J. Mammal. 71, 188–194 (1990).Article 

Google Scholar 
18.Saunders, G., White, P. C. L., Harris, S. & Rayner, J. M. V. Urban foxes (Vulpes vulpes)—Food acquisition, time and energy budgeting of a generalized predator. Symp. Zool. Soc. Lond. 65, 215–234 (1993).
Google Scholar 
19.Contesse, P., Hegglin, D., Gloor, S., Bontadina, F. & Deplazes, P. The diet of urban foxes (Vulpes vulpes) in the city of Zurich, Switzerland. Mamm. Biol. 69, 81–95 (2004).Article 

Google Scholar 
20.Harris, S. An estimation of the number of foxes (Vulpes vulpes) in the city of Bristol and some possible factors affecting their distribution. J. Appl. Ecol. 18, 455–465 (1981).Article 

Google Scholar 
21.Marks, C. A. & Bloomfield, T. E. Distribution and density estimates for urban foxes (Vulpes vulpes) in Melbourne: Implications for rabies control. Wildl. Res. 26, 763–775 (1999).Article 

Google Scholar 
22.Gloor, S. The rise of urban foxes (Vulpes vulpes) in Switzerland and ecological and parasitological aspects of a population in the recently colonised city of Zurich. Dissertation thesis (University of Zurich, 2002).23.Gosselink, T. E., van Deelen, T. R., Warner, B. E. & Joselyn, M. G. Temporal habitat partitioning and spatial use of coyotes and red foxes in east-central Illinois. J. Wildl. Manag. 55, 433–441 (2003).
Google Scholar 
24.Gosselink, T. E., van Deelen, T. R., Warner, R. E. & Mankin, P. C. Survival and cause-specific mortality of red foxes in agricultural and urban areas of Illinois. J. Wildl. Manag. 7, 1862–1873 (2007).Article 

Google Scholar 
25.Soulsbury, C. D. et al. The impact of sarcoptic mange Sarcoptes scabiei on the British fox Vulpes vulpes population. Mammal Rev. 37, 278–296 (2007).
Google Scholar 
26.Macdonald, D. Running with the Fox (Unwin Hyman, 1987).
Google Scholar 
27.Lewis, J. C., Sallee, K. L. & Golightly, Jr R. T. Introduced red fox in California. http://morro-bay.com/educational/research-reports/red-fox–california-introduced-research-93_10.pdf (1993).28.Plumer, L., Davison, J. & Saarma, U. Rapid urbanization of red foxes in Estonia: Distribution, behaviour, attacks on domestic animals and health-risks related to zoonotic diseases. PLoS ONE 9, e115124. https://doi.org/10.1371/journal.pone.0115124 (2014).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
29.Sogliani, D. & Mori, E. ‘The Fox and the Cat’: Sometimes they do not agree. Mamm. Biol. 95, 150–154 (2019).Article 

Google Scholar 
30.König, A. Fears, attitudes and opinions of suburban residents with regards to their urban foxes. Eur. J. Wildl. Res. 54, 101–109 (2008).Article 

Google Scholar 
31.Kauhala, K., Talvitie, K. & Vuorisalo, T. Encounters between medium-sized carnivores and humans in the city of Turku, SW Finland, with special reference to the red fox. Mammal Res. 61, 25–33 (2016).Article 

Google Scholar 
32.Teagle, W. G. The fox in the London suburbs. Lond. Nat. 46, 44–68 (1967).
Google Scholar 
33.Pagh, S. The history of urban foxes in Aarhus and Copenhagen, Denmark. Lutra 51, 51–55 (2008).
Google Scholar 
34.Vuorisalo, T., Talvitie, K., Kauhala, K., Blauerc, A. & Lahtinene, R. Urban red foxes (Vulpes vulpes L.) in Finland: A historical perspective. Landsc. Urban Plan. 124, 109–117 (2014).Article 

Google Scholar 
35.Seebeck, J. H. Mammals in the Melbourne metropolitan area. Vic. Nat. 94, 165–171 (1977).
Google Scholar 
36.Gloor, S., Bontadina, F., Hegglin, D., Deplazes, P. & Breitenmoser, U. The rise of urban fox populations in Switzerland. Mamm. Biol. 66, 155–164 (2001).
Google Scholar 
37.Soulsbury, C. D., Baker, P. J., Iossa, G. & Harris, S. Red foxes (Vulpes vulpes). In Urban Carnivores Ecology, Conflict, and Conservation (eds Gehrt, S. D. et al.) 63–75 (The Johns Hopkins University Press, 2010).
Google Scholar 
38.Chautan, M., Pontier, D. & Artois, M. The role of rabies in recent demographic changes in red fox populations in Europe. Mammalia 46, 391–410 (2000).
Google Scholar 
39.Doncaster, C. P. & MacDonald, D. W. Activity patterns and interactions of red fox (Vulpes vulpes) in Oxford city. J. Zool. 241, 73–87 (1997).Article 

Google Scholar 
40.Harris, S. Surveying the urban fox. Biologist 35, 259–264 (1985).
Google Scholar 
41.Uraguchi, K., Yamamura, K. & Saitoh, T. Estimating number of families for an urban fox population by using two public data sets. Popul. Ecol. 51, 1–7 (2009).Article 

Google Scholar 
42.Scott, D. M. et al. A citizen science based survey method for estimating the density of urban carnivores. PLoS ONE 13, e0197445. https://doi.org/10.1371/journal.pone.0197445 (2018).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
43.Sadlier, L. M. J., Webbon, C. C., Baker, P. J. & Harris, S. Methods of monitoring red foxes Vulpes vulpes and badgers Meles meles: Are field signs the answer?. Mammal Rev. 34, 75–98 (2004).Article 

Google Scholar 
44.Baker, P. J., Harris, S., Robertson, C. P. J., Saunders, G. & White, P. C. L. Is it possible to monitor mammal population changes from counts of road traffic casualties? An analysis using Bristol’s red foxes Vulpes vulpes as an example. Mammal Rev. 34, 115–130 (2004).Article 

Google Scholar 
45.Statistics Poland. Statistical Yearbook of Warsaw (Zakład Wydawnictw Statystycznych, 2019).
Google Scholar 
46.Climate-data.org. https://pl.climate-data.org/europa/polska/masovian-voivodeship/warszawa-4560/ (2020).47.Goszczyński, J. & Romanowski, J. The mammals of the between-floodbanks area of the Middle Vistula Valley. In The Between Floodbanks Area of the Vistula as an Unique Natural System (Pilica-Narew section) (eds Matuszkiewicz, J. M. & Roo-Zielińska, E.) 107–117 (Polish Academy of Sciences, 2000).
Google Scholar 
48.Romanowski, J. Vistula River valley as the ecological corridor for mammals. Pol. J. Ecol. 55, 805–819 (2007).
Google Scholar 
49.Romanowski, J., Kowalczyk, K. & Rau, K. Population viability modelling and potential threats to the beaver in the Vistula River valley, Poland. Ann. Zool. Fenn. 45, 323–328 (2008).Article 

Google Scholar 
50.Luniak, M., Kozłowski, P. & Nowicki, W. Magpie Pica pica in Warsaw—abundance, distribution and changes in its population. Acta Ornithol. 32, 77–86 (1997).
Google Scholar 
51.Gryz, J., Lesiński, G., Krauze-Gryz, D. & Stolarz, P. Woodland reserves within an urban agglomeration as important refuges for small mammals. Folia For. Pol. Ser. A For. 59, 3–13 (2017).
Google Scholar 
52.Sison, C. P. & Glaz, J. Simultaneous confidence intervals and sample size determination for multinomial proportions. J. Am. Stat. Assoc. 90, 366–369 (1995).MathSciNet 
MATH 
Article 

Google Scholar 
53.Signorell, A. et al. DescTools: Tools for descriptive statistics. R package version 0.99. 26. The Comprehensive R Archive Network (2018).54.Wood, S. N. Generalized Additive Models: An Introduction with R (Chapman and Hall/CRC, 2006).MATH 
Book 

Google Scholar 
55.Wood, S. N. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models: Estimation of semiparametric generalized linear models. J. R. Stat. Soc. Ser. B Stat. Methodol. 73, 3–36 (2011).MathSciNet 
MATH 
Article 

Google Scholar 
56.Copernicus ,. Mapping Guide for an European Urban Atlas (European Union, 2018).
Google Scholar 
57.R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).
Google Scholar 
58.ESRI. ArcGIS Desktop: Release 10 (Enviromental Systems Research Institute, 2011).
Google Scholar 
59.Wałecki, A. Fauna zwierząt ssących Warszawy i jej stosunek do fauny całego kraju in Pamiętnik Fizjograficzny Vol. 1, 268–291 (E. Dziewulski i Br. Znatowicz, 1881).
Google Scholar 
60.Wandeler, P., Funk, S. M., Largiader, C. R., Gloor, S. & Breitenmoster, U. The city-fox phenomenon: Genetic consequences of a recent colonization of urban habitat. Mol. Ecol. 12, 647–656 (2003).CAS 
PubMed 
Article 

Google Scholar 
61.DeCandia, A. L. et al. Urban colonization through multiple genetic lenses: The city-fox phenomenon revisited. Ecol. Evol. 9, 2046–2060 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
62.Kimmig, S. E. et al. Beyond the landscape: Resistance modelling infers physical and behavioural gene flow barriers to a mobile carnivore across a metropolitan area. Mol. Ecol. 29, 466–484 (2020).PubMed 
Article 

Google Scholar 
63.Kato, Y. et al. Population genetic structure of the urban fox in Sapporo, northern Japan. J. Zool. 301, 118–124 (2017).Article 

Google Scholar 
64.Baker, P. J., Dowding, C. V., Molony, S. E., White, P. C. L. & Harris, S. Activity patterns of urban red foxes (Vulpes vulpes) reduce the risk of traffic-induced mortality. Behav. Ecol. 18, 716–724 (2007).Article 

Google Scholar 
65.Gehrt, S. D. The urban ecosystem. In Urban Carnivores Ecology, Conflict, and Conservation (eds Gehrt, S. D. et al.) 3–11 (The Johns Hopkins University Press, 2010).
Google Scholar 
66.Kolb, H. H. Factors affecting the movements of dog foxes in Edinburgh. J. Appl. Ecol. 21, 161–173 (1984).Article 

Google Scholar 
67.Douglas, I. & Sadler, J. P. Urban wildlife corridors. Conduits for movement or linear habitats? In The Routledge Handbook of Urban Ecology (eds Douglas, I. et al.) 274–288 (Routledge, 2011).
Google Scholar 
68.Tsukada, H., Morishima, Y., Nonaka, N., Oku, Y. & Kamiya, M. Preliminary study of the role of red foxes in Echinococcus multilocularis transmission in the urban area of Sapporo, Japan. Parasitology 120, 423–428 (2000).PubMed 
Article 

Google Scholar 
69.Robinson, N. A. & Marks, C. A. Genetic structure and dispersal of red foxes (Vulpes vulpes) in urban Melbourne. Aust. J. Zool. 49, 589–601 (2001).Article 

Google Scholar 
70.Walter, T., Zink, R., Laaha, G., Zaller, J. G. & Heigl, F. Fox sightings in a city are related to certain land use classes and sociodemographics: Results from a citizen science project. BMC Ecol. 18, 50. https://doi.org/10.1186/s12898-018-0207-7 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
71.Cavallini, P. & Lovari, S. Home range, habitat selection and activity of the red fox in a Mediterranean coastal ecotone. Acta Theriol. 39, 279–287 (1994).Article 

Google Scholar 
72.Frey, S. N. & Conover, M. R. Habitat use by meso-predators in a corridor environment. J. Wildl. Manag. 70, 1111–1118 (2006).Article 

Google Scholar 
73.Díaz-Ruíz, F., Caro, J., Delibes-Mateos, M., Arroyo, B. & Ferreras, P. Drivers of red fox (Vulpes vulpes) daily activity: Prey availability, human disturbance or habitat structure?. J. Zool. 298, 128–138 (2016).Article 

Google Scholar 
74.Gaffron, P. Urban transport, environmental justice and human daily activity patterns. Transp. Policy 20, 114–127 (2012).Article 

Google Scholar 
75.Eguchi, K. & Nakazano, T. Activity studies of Japanese red foxes, Vulpes vulpes japonica Gray. Jpn. J. Ecol. 30, 9–17 (1980).
Google Scholar 
76.Travaini, A., Aldama, J. J., Laffitte, R. & Delibes, M. Home range and activity patterns of red fox Vulpes vulpes breeding females. Acta Theriol. 38, 427–434 (1993).Article 

Google Scholar 
77.Cavallini, P. Ranging behaviour of red foxes during the mating and breeding seasons. Ethol. Ecol. Evol. 8, 57–65 (1996).Article 

Google Scholar 
78.Robertson, C. P. J., Baker, P. J. & Harris, S. Ranging behaviour of juvenile red foxes and its implications for management. Acta Theriol. 45, 525–535 (2000).Article 

Google Scholar 
79.Goszczyński, J. Lis. Monografia przyrodniczo-łowiecka (OIKOS Oficyna Wydawnicza, 1995).
Google Scholar 
80.Tolhurst, B. A., Baker, R. J., Cagnacci, F. & Scott, D. M. Spatial aspects of gardens drive ranging in urban foxes (Vulpes vulpes): The resource dispersion hypothesis revisited. Animals 10, 1167. https://doi.org/10.3390/ani10071167 (2020).Article 
PubMed Central 
PubMed 

Google Scholar 
81.Hofer, S. et al. High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology 120, 135–142 (2000).PubMed 
Article 

Google Scholar 
82.Jiang, S., Ferreira, Jr J. & Gonzalez, M. C. Discovering urban spatial–temporal structure from human activity patterns. In Proceedings of the ACM SIGKDD International Workshop on Urban Computing (UrbComp ’12) (ACM New York, 2012).83.Newman, T. J. et al. Changes in red fox habitat preference and rest site fidelity following a disease-induced population decline. Acta Theriol. 48, 79–91 (2003).Article 

Google Scholar 
84.Fischer, C., Reperant, L., Weber, J. M., Ochs, H. & Deplazes, P. Relation in the presence of various parasites in the red fox (Vulpes vulpes) in Geneva. Swiss Med. Wkly. 133, 61 (2003).
Google Scholar 
85.Deplazes, S., Hegglin, D., Gloor, S. & Romig, T. Wilderness in the city: The urbanization of Echinococcus multilocularis. Trends Parasitol. 20, 77–84 (2004).PubMed 
Article 

Google Scholar 
86.Official Website of Republic of Poland. https://www.gov.pl/web/uw-mazowiecki/obszar-zagrozony-wscieklizna-na-terenie-wojewodztwa-mazowieckiego (2021).87.Wilkinson, D. & Smith, G. C. A preliminary survey for changes in urban fox (Vulpes vulpes) densities in England and Wales, and implications for rabies control. Mammal Rev. 31, 107–110 (2001).Article 

Google Scholar 
88.Baker, P. J., Funk, S. M., Harris, S. & White, P. C. L. Flexible spatial organization of urban foxes, Vulpes vulpes, before and during an outbreak of sarcoptic mange. Anim. Behav. 59, 127–146 (2000).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
89.Goszczyński, J. The effect of structural differentation of ecological landscape on the predator–prey interaction. Treatises Monogr. 46, 1–80 (1985).
Google Scholar 
90.Goszczyński, J., Misiorowska, M. & Juszko, S. Changes in the density and spatial distribution of red fox dens and cub numbers in central Poland following rabies vaccination. Acta Theriol. 53, 121–127 (2008).Article 

Google Scholar  More

CORRESPONDENCE
06 July 2021

Protect pollinators — reform pesticide regulations

Adrian Fisher

 ORCID: http://orcid.org/0000-0001-5300-1910

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Adrian Fisher

Arizona State University, Tempe, Arizona, USA. On behalf of 14 co-signatories.

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Many approved pesticides still damage pollinator health at doses used in agriculture (see, for example, A. R. Main et al. Agric. Ecosyst. Environ. 287, 106693; 2020). We argue that this is due to a systemic failure in pesticide regulations (see, for instance, S. López-Cubillos et al. Nature 573, 196; 2019) that has been exacerbated by weak enforcement. Stricter laws are needed that are evidence-based, override vested interests and recognize pollinators as essential contributors to food security.Policymakers must learn from failures in neonicotinoid regulation (see, for example, F. Sgolastra et al. Biol. Conserv. 241, 108356; 2020). Before approval, pesticide risk assessment should incorporate protocols that address sub-lethal effects on pollinators. These include alterations in their behaviour and fitness under ecologically realistic conditions; mandatory testing on diverse species of native pollinators and of colonies for eusocial pollinators; and toxicity evaluation when combined with other chemicals such as proprietary additives, co-occurring pesticides and environmental residues.Long-term monitoring after approval by appropriate governmental organizations will be necessary to pick up unforeseen environmental interactions promptly.

Nature 595, 172 (2021)
doi: https://doi.org/10.1038/d41586-021-01818-xA full list of co-signatories to this letter appears in Supplementary Information.

Supplementary Information

List of co-signatories

Competing Interests
The authors declare no competing interests.

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