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    Rapid evolution of an adaptive taste polymorphism disrupts courtship behavior

    Cockroach strainsAll cockroaches were maintained on rodent diet (Purina 5001, PMI Nutrition International, St. Louis, MO) and distilled water at 27 °C, ~40% RH, and a 12:12 h L:D cycle. The WT colony (Orlando Normal) was collected in Florida in 1947 and has served as a standard insecticide-susceptible strain. The GA colony (T-164) was collected in 1989, also in Florida, and shown to be aversive to glucose; continued artificial selection with glucose-containing toxic bait fixed the homozygous GA trait in this population (approximately 150 generations as of 2020).Generating recombinant lines and life history dataTo homogenize the genetic backgrounds of the WT and GA strains, two recombinant colonies were initiated in 2013 by crossing 10 pairs of WT♂ × GA♀ and 10 pairs of GA♂ × WT♀ (Fig. 3a). At the F8 generation (free bulk mating without selection), 400 cockroaches were tested in two-choice feeding assays (see below) that assessed their initial response to tastants, as described in previous studies11,26. The cockroaches were separated into glucose-accepting and glucose-rejecting groups by the rapid Acceptance-Rejection assay (described in Feeding Bioassays). These colonies were bred for three more generations, and 200 cockroaches from each group were assayed in the F11 generation and backcrossed to obtain homozygous glucose-accepting (aa) and glucose-averse (AA) lines. Similar results were obtained in both directions of the cross, confirming previous findings of no sex linkage of the GA trait27. These two lines were defined as WT_aa (homozygotes, glucose-accepting) and GA_AA (homozygotes, glucose-averse). To obtain heterozygous GA cockroaches, GA_Aa, a single intercross group was generated from crosses of 10 pairs of WT_aa♂ × GA_AA♀ and 10 pairs of GA_AA♂ × WT_aa♀.The GA trait follows Mendelian inheritance. Therefore, we used backcrosses, guided by two-choice feeding assays and feeding responses in Acceptance-rejection assays, to determine the homozygosity of WT and GA cockroaches. The cross of WT♂ × WT♀ produced homozygous F1 cockroaches showing maximal glucose-acceptance. The cross of GA♂ × GA♀ produced homozygous F1 cockroaches showing maximal glucose-aversion. The cross of WT × GA produced F1 heterozygotes with intermediate glucose-aversion. When the F1 heterozygotes were backcrossed with WT cockroaches, they produced F2 cockroaches with a 1:1 ratio of WT and GA phenotypes.The two-choice feeding assay assessed whether cockroaches accepted or rejected glucose (binary: yes-no). Insects were held for 24 h without water, or starved without food and water. Either 10 adults or 2 day-old first instar siblings (30–40) were placed in a Petri dish (either 90 mm or 60 mm diameter × 15 mm height). Each Petri dish contained two agar discs: one disc contained 1% agar and 1 mmol l−1 red food dye (Allura Red AC), and the second disc contained 1% agar, 0.5 mmol l−1 blue food dye (Erioglaucine disodium salt) and either 1000 mmol l−1 or 3000 mmol l−1 glucose. The assay duration was 2 h during the dark phase of the insects’ L:D cycle. After each assay, the color of the abdomen of each cockroach was visually inspected under a microscope to infer the genotype.We assessed whether the recombinant colonies had different traits from the parental WT and GA lines. We paired single newly eclosed females (day 0) with single 10–12 days-old males of the same line in a Petri dish (90 mm diameter, 15 mm height) with fresh distilled water in a 1.5 ml microcentrifuge tube and a pellet of rodent food, and monitored when they mated. When females formed egg cases, each gravid female was placed individually in a container (95 × 95 × 80 mm) with food and water until the eggs hatched. After removing the female, her offspring were monitored until adult emergence. We recorded the time to egg hatch, first appearance of each nymphal stage, first appearance of adults and the end of adult emergence. The first instar nymphs and adults in each cohort were counted to obtain measures of survivorship. Although there were significant differences in some of these parameters across all four strains, we found no significant differences between the two recombinant lines, except mating success, which was significantly lower in GA_AA♀ than WT_aa♀ (Supplementary Table 11).Mating bioassaysAll mating sequences were recorded using an infra-red-sensitive camera (Polestar II EQ610, Everfocus Electronics, New Taipei City, Taiwan) coupled to a data acquisition board and analyzed by searchable and frame-by-frame capable software (NV3000, AverMedia Information) at 27 °C, ~40% RH and a 12:12 h L:D cycle. For behavioral analysis, tested pairs were classified into two groups: mated (successful courtship) and not-mated (failed courtship). Four distinct behavioral events (Fig. 1c, Contact, Wing raising, Nuptial feeding, and Copulation) were analyzed using seven behavioral parameters as shown in Supplementary Table 2.We extracted behavioral data from successful courtship sequences, defined as courtship that led to Copulation. For failed courtship sequences, we extracted the behavioral data from the first courtship of both mated and not-mated groups, because most pairs in both groups failed to copulate in their first encounter, and there were no significant differences in behavioral parameters between the two groups.To assay female choice, we conducted two-choice mating assays (Fig. 1a). A single focal WT♀ or GA♀ and two males, one WT and one GA, were placed in a Petri dish (90 mm diameter, 15 mm height) with fresh distilled water in a 1.5 ml microcentrifuge tube and a pellet of rodent food (n = 25 WT♀ and 27 GA♀). To assay male choice, a single focal WT♂ or GA♂ was given a choice of two females, one WT♀ and one GA♀ (n = 27 WT♂ and 18 GA♂). Experiments were started using 0 day-old sexually unreceptive females and 10–12 days-old sexually mature males. Newly emerged (0 day-old) females were used to avoid the disruption of introducing a sexually mature female into the bioassay. B. germanica females become sexually receptive at 5–7 days of age, so the mating behavior of the focal insect was video-recorded for several days until they mated. Fertility of mated females was evaluated by the number of offspring produced. We assessed the gustatory phenotype of nymphs (either WT-type or GA-type) to determine which of the two adult cockroaches mated with the focal insect. Each gravid female was maintained individually in a container (95 × 95 × 80 mm) with food and water until the eggs hatched. Two day-old first instar nymphs were starved for one day without water and food, and then they were tested in Two-choice feeding assays using 1000 mmol l−1 glucose-containing agar with 0.5 mmol l−1 blue food dye vs. plain sugar-free agar with 1 mmol l−1 red food dye. If all the nymphs chose the glucose-containing agar, their parents were considered WT♂ and WT♀. When all the nymphs showed glucose-aversion, they were raised to the adult stage. Newly emerged adults were backcrossed with WT cockroaches, and their offspring were tested in the Two-choice assay. When the parents were both GA, 100% of the offspring exhibited glucose-aversion. When the parents were WT and GA, the offspring showed a 1:1 ratio of glucose-accepting and glucose-aversive behavior. Mate choice, mating success ratio and the number of offspring were analyzed statistically.We conducted no-choice mating assay using the WT and GA strains (Fig. 1b, d). A female and a male were placed in a Petri dish with fresh water and a piece of rodent food and video-recorded for 24 h. The females were 5–7 days-old and males were 10–12 days-old. Four treatment pairs were tested: WT♂ × WT♀ (n = 20, 18 and 14 pairs for 5, 6 and 7 day-old females, respectively); GA♂ × GA♀ (n = 23, 22 and 35 pairs); GA♂ × WT♀ (n = 21, 14 and 17 pairs); and WT♂ × GA♀ (n = 33, 19 and 15 pairs).To confirm that gustatory stimuli guide nuptial feeding, we artificially augmented the male nuptial secretion and assessed whether the duration of nuptial feeding and mating success of GA♀ were affected (Fig. 2c). Before starting the mating assay with 5 day-old GA♀, 10–12 days-old WT♂ were separated into three groups: A control group did not receive any augmentation; A water control group received distilled water with 1 mmol l−1 blue dye (+Blue); A fructose group received 3000 mmol l−1 fructose solution with blue dye (+Blue+Fru). Approximately 50 nl of the test solution was placed into the tergal gland reservoirs using a glass microcapillary. No-choice mating assays were carried out for 24 h. n = 20–25 pairs for each treatment.We evaluated the association of short nuptial feeding (Fig. 1c) and the GA trait we conducted no-choice mating assays using females from the recombinant lines (Fig. 3c). Before starting each mating assay with 4 day-old females from the WT, GA and recombinant lines (WT_aa, GA_AA and GA_Aa), the EC50 for glucose was obtained by the instantaneous Acceptance-Rejection assay using 0, 10, 30, 100, 300, 1000 and 3000 mmol l−1 glucose (WT♀ and WT_aa♀, non-starved; GA♀, GA_AA♀ and GA_Aa♀, 1-day starved). After the Acceptance-Rejection assay, GA_Aa♀ were separated into two groups according to their sensitivity for rejecting glucose; the GA_Aa_high sensitivity group rejected glucose at 100 and 300 mmol l−1, whereas the GA_Aa_low sensitivity group rejected glucose at 1000 and 3000 mmol l−1. We paired these females with 10–12 days-old WT♂ (n = 15 WT_aa♀, n = 20 GA_AA♀, n = 20 GA_Aa_high♀ and n = 17 GA_Aa_low♀).Feeding bioassayWe conducted two feeding assays: Acceptance-Rejection assay and Consumption assay. The Acceptance-Rejection assay assessed the instantaneous initial responses (binary: yes-no) of cockroaches to tastants, as previously described7,22,27. Briefly, acceptance means that the cockroach started drinking. Rejection means that the cockroach never initiated drinking. The percentage of positive responders was defined as the Number of insects accepting tastants/Total number of insects tested. The effective concentration (EC50) for each tastant was obtained from dose-response curves using this assay. The Consumption assay was previously described27. Briefly, we quantified the amount of test solution females ingested after they started drinking. Females were observed until they stopped drinking, and we considered this a single feeding bout.We used the Acceptance-Rejection assay and Consumption assay, respectively, to assess the sensitivity of 5 day-old WT♀ and GA♀ for accepting and consuming the WT♂ nuptial secretion (Fig. 2a, b). The secretion was diluted with HPLC-grade water to 0.001, 0.01, 0.03, 0.1, 0.3 and 1 male-equivalents/µl (n = 20 non-starved females each). The amount of nuptial secretion consumed was tested at 0.1 male-equivalents/µl in the Consumption assay (n = 10 each).The Acceptance-Rejection assay was used to calculate the effective concentration (EC50) of glucose for females in the WT, GA and recombinant lines (Fig. 3a, b). A glucose concentration series of 0.1, 1, 10, 100 and 1000 mmol l−1 was tested with one-day starved 4-day old females (n = 65 GA_Aa♀, n = 50 GA_AA♀ and n = 50 GA♀) and non-starved females (n = 50 WT_aa♀ and n = 16 WT♀).The effects of female saliva on feeding responses of 5 day-old WT♀ and GA♀ were tested using the Acceptance-Rejection assay (Fig. 4a). Freshly collected saliva of WT♀ and GA♀ was immediately used in experiments. Assays were prepared as follows: 3 µl of 200 mmol l−1 maltose or maltotriose were mixed with 3 µl of either HPLC-grade water or saliva of WT♀ or GA♀. The final concentration of each sugar was 100 mmol l−1 in a total volume of 6 µl. This concentration represented approximately the acceptance EC70 for WT♀ and GA♀27. Nuptial secretion (1 µl representing 10 male-equivalents) was mixed with 1 µl of either HPLC-grade water or saliva from WT♀ or GA♀, and 8 µl of HPLC-grade water was added to the mix. The final concentration of the nuptial secretion was 1 male-equivalent/µl in a total volume of 10 µl. This concentration also represented approximately the acceptance EC70 for WT♀ and GA♀ (Fig. 2a). The mix of saliva and either sugar or nuptial secretion was incubated for 300 s at 25 °C. Additionally, we tested the effect of only saliva in the Acceptance-Rejection assay. Either 1-day starved or non-starved females were tested with water only and then a 1:1 mixture of saliva and water. Saliva alone did not affect acceptance or rejection of stimuli. n = 20–33 females from each strain.To evaluate whether salivary enzymes are involved in the hydrolysis of oligosaccharides, the contribution of salivary glucosidases was tested using the glucosidase inhibitor acarbose in the Acceptance-Rejection assay (Fig. 4b), as previously described27. We first confirmed that the range of 0–125 mmol l−1 acarbose in HPLC-grade water did not disrupt the acceptance and rejection of tastants. Test solutions were prepared as follows: 2 µl of either HPLC-grade water or saliva of GA♀ was mixed with 1 µl of either 250 µmol l−1 of acarbose or HPLC-grade water, then the mixture was added to 1 µl of 400 mmol l−1 of either maltose or maltotriose solution. The total volume was 4 µl, with the final concentration of sugar being 100 mmol l−1. For assays with nuptial secretion, 1 µl of either HPLC-grade water or saliva from 5 day-old GA♀ was mixed with 0.5 µl of either 250 µmol l−1 of acarbose or HPLC-grade water. This mixture was added to 0.5 µl of 10 male-equivalents of nuptial secretion (i.e., 20 male-equivalents/µl). HPLC-grade water was added for a total volume of 10 µl and a final concentration of 1 male-equivalent/µl. The mix of saliva and either sugars or nuptial secretion was incubated for 5 min at 25 °C. All test solutions contained blue food dye. Test subjects were 5 day-old GA♀ and 20–25 females were tested in each assay.Nuptial secretion and saliva collectionsThe nuptial secretion of WT♂ was collected by the following method: Five 10–12 days-old males were placed in a container (95 × 95 × 80 mm) with 5 day-old GA♀. After the males displayed wing-raising courtship behavior toward the females, individual males were immediately decapitated and the nuptial secretion in their tergal gland reservoirs was drawn into a calibrated borosilicate glass capillary (76 × 1.5 mm) under the microscope. The nuptial secretions from 30 males were pooled in a capillary and stored at −20 °C until use. Saliva from 5 day-old WT♀ and GA♀ was collected by the following method: individual females were briefly anesthetized with carbon dioxide under the microscope and the side of the thorax was gently squeezed. A droplet of saliva that accumulated on the mouthparts was then collected into a microcapillary (10 µl, Kimble Glass). Fresh saliva was immediately used in experiments.GC-MS procedures for analysis of sugarsStandards of D-( + )-glucose (Sigma-Aldrich), D-( + )-maltose (Fisher Scientific) and maltotriose (Sigma-Aldrich) were diluted in HPLC-grade water (Fisher Scientific) at 10, 50, 100, 500 and 1000 ng/µl to generate calibration curves. Samples were vortexed for 20 s and a 10 μl aliquot of each sample was transferred to a Pyrex reaction vial containing a 10 μl solution of 5 ng/μl sorbitol (≥98%) in HPLC-grade water as internal standard and dried under a gentle flow of N2 for 20 min.Samples containing degradation products from nuptial secretions were prepared by adding 15 μl of HPLC-water to each sample in a 1.5 ml Eppendorf tube, vortexed for 30 s and centrifuged at 8000 rpm (5223 RCF) for 5 min to separate lipids from the water layer. The water phase was transferred to a reaction vial using a glass capillary. This procedure was repeated with the remaining lipid layer and the water layers were combined in the same reaction vial containing 10 μl of a solution of 5 ng/μl sorbitol and dried under N2 for 20 min.For derivatization of sugars and samples, each reaction vial received 12 μl of anhydrous pyridine under a constant N2 flow, then vortexed and incubated at 90 °C for 5 min. Three μl of N-methyl-N-(trimethylsilyl)trifluoroacetamide (MSTFA; Sigma-Aldrich) was added to each reaction vial and centrifuged at 1000 rpm (118 RCF) for 2 min. Vials were incubated in a heat block at 90 °C for 1.5 hr and vortexed every 10 min for the first 30 min of incubation.The total volume of sample was ~10 μl, and 1 μl was injected into the GC-MS (6890 GC coupled to a 5975 MS, Agilent Technologies, Palo Alto, CA). The inlet was operated in splitless mode (17.5 psi) at 290 °C. The GC was equipped with a DB-5 column (30 m, 0.25 mm, 0.25 μm, Agilent), and helium was used as the carrier gas at an average velocity of 50 cm/s. The oven temperature program started at 80 °C for 1 min, increased at 10 °C/min to 180 °C, then increased at 5 °C/min to 300 °C, and held for 10 min. The transfer line was set at 250 °C for 24 min, ramped at 5 °C/min to 300 °C and held until the end of program. The ion source operated at 70 eV and 230 °C, while the MS quadrupole was maintained at 200 °C. The MSD was operated in scan mode, starting after 9 min (solvent delay time) with a mass range of 33–650 AMU.For GC-MS data analysis, the sorbitol peak area was obtained from the extracted ion chromatograms with m/z = 205, the sorbitol base peak. The area of peaks of glucose, maltose and maltotriose were obtained from the extracted ion chromatograms using m/z = 204, the base peak of the three sugars. The most abundant peaks of each sugar were selected for quantification36, and these peaks did not coelute with other peaks. Then, the peak areas of the three sugars were divided by the area of the respective sorbitol peak in each sample to normalize the data and to correct technical variability during sample processing. This procedure was performed to obtain the calibration curves and quantification of sugars in our experiments.The results of sugar analysis using GC-MS are reported in Supplementary Figs. 1–4.Analysis of nuptial secretionsWe focused the GC-MS analysis on glucose, maltose and maltotriose in WT♂ nuptial secretion (Fig. 4c). To quantify the time-course of saliva-catalyzed hydrolysis of WT♂ nuptial secretion to glucose, 1 µl of GA♀ saliva was mixed with 1 µl of 10 male-equivalents/µl. We incubated the mixtures for 0, 5, 10 and 300 s at 25 °C, and added 4 µl of methanol to stop the enzyme activity (n = 5 each treatment). Each sample contained the nuptial secretions of 5 males to obtain enough detectable amount of sugars. For the statistical analysis, the amounts of sugars were divided by 5 to obtain the amount of sugars in 1 male (1 male-equivalent). These amounts were also used for generating Fig. 4c and Supplementary Table 9. In calculations of the concentration of the three sugars (mmol l−1), the mass and volume of the nuptial secretion were measured using 70–130 male-equivalents of undiluted secretion of each strain (n = 3). The mass and volume of the nuptial secretion/male, including both lipid and aqueous layers, were approximately 30–50 µg and 40–50 nl. Because it was difficult to separate the lipid layer from the water layer at this small scale, we roughly estimated that the tergal reservoirs of the four cockroach lines had 30 nl of aqueous layer that contained sugars.To quantify the time-course of saliva-catalyzed hydrolysis of maltose and maltotriose to glucose, 1 µl of GA♀ saliva was mixed with 1 µl of 200 mmol l−1 of either maltose or maltotriose (Fig. 4d, e). Incubation time points were 0, 5, 10 and 300 s at 25 °C and methanol was used to stop the enzyme activity. Controls without saliva were also prepared using HPLC-grade water instead of saliva and 300 s incubations. n = 5 for each treatment.PhotomicroscopyThe photographs of the tergal glands and mouthparts (Fig. 5) were obtained using an Olympus Digital camera attached to an Olympus CX41 microscope (Olympus America, Center Valley, PA).Statistics and reproducibilityThe sample size and number of replicates for each experiment are noted in the respective section describing the experimental details. In summary, the samples sizes were: Mating bioassays, n = 18–80; Feeding assays, n = 16–65; Sugar analysis, n = 5; Life history parameters, n  > 14. All statistical analyses were conducted in R Statistical Software (v4.1.0; R Core Team 2021) and JMP Pro 15.2 software (SAS Institute Inc., Carey, NC). For bioassay data and sugar analysis data, we calculated the means and standard errors, and we used the Chi-square test with Holm’s method for post hoc comparisons, t-test, and ANOVA followed by Tukey’s HSD test (all α = 0.05), as noted in each section describing the experimental details, results, and in Supplementary Tables 1–11.Reporting summaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

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    International food trade benefits biodiversity and food security in low-income countries

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    Habitat Protection Indexes – new monitoring measures for the conservation of coastal and marine habitats

    There are 23 international conventions related to protecting the marine environment and biodiversity, with five of these requiring the implementation of marine protected areas27. Targets for the effective protection of marine habitats that conserve nature and secure nature’s contributions to people are increasingly seen as critical in ensuring progress toward meeting treaty commitments. Aichi Target 11 and the Sustainable Development Goals Target 14.5 aim to conserve at least 10% of marine and coastal areas by 2020, reflecting a shift to a more target-driven conservation policy at the international level, although this is hotly debated. Warm-water corals, mangroves, and saltmarshes all have more than 30% of their extent within PCAs, with seagrasses and cold-water corals approaching 30%, which reveals a dedicated effort to their conservation of these critical habitats. However, the protection of the total global ocean area is still at 7.92%, with only 1.18% of ABNJ covered by PCAs, falling short of the 10% of Aichi Target 11 previously set for 202016.Standardized and open source tools and platforms are needed to allow robust monitoring of progress towards international targets. While tools are available to measure advancement in some targets24,25,26, fully replicable workflows that guide the user from data preparation to index calculations have been lacking. The workflow presented here provides one of the first steps to fill this gap. The indexes also give a global context for the conservation of the habitats, highlighting ecological representation and individual jurisdictions’ potential to contribute to future conservation efforts. Combining our indexes with other tools, such as spatial conservation planning, allows policymakers to balance tradeoffs with different priorities, such as climate mitigation and resource extraction (e.g.13).While our indexes do not measure the “equitably managed” component of the Aichi target 11, it is critical that a holistic, human rights-based approach is taken in meeting any targets set and efforts to improve biodiversity outcomes. The consideration of human rights of local communities and indigenous people and inclusion of their voices is absolutely necessary in the decision-making process28.Interpretation and Usefulness of the Workflow and IndexesThe LPHPI and GPHPI are consistent ways of measuring progress in establishing protected areas that have the potential to conserve habitats and biodiversity. Additionally, the completely open access workflow described in Fig. 5 is highly adaptable and can include a wide range of habitats as data become available, or it can be applied to different conservation features like species distributions. The workflow could also be adapted to calculate the amount of key biodiversity areas within PCAs per jurisdiction and globally, or human threats (e.g., pollution or heatwaves) when geospatial data is available. Notably, the workflow can also measure progress towards targets in the draft post-2020 global biodiversity framework (as of August 2020).Fig. 5A flow chart describing the key steps of the indexes calculations. We also connect each step to the R script available at: https://github.com/jkumagai96/Marine_Habitat_protection where a more detailed explanation on how to replicate the workflow is available.Full size imageSpecifically, the workflow and resulting LPHPI dataset can directly monitor the marine components T2.1 and T2.3 of Target 2 of the draft monitoring framework (reproduced in Table 1 for convenience). The workflow can also be easily adapted to calculate the freshwater and terrestrial aspects of Target 2 – component T2.1 and component T2.2. The Protected Area Representativeness Index and Species Protection Index currently proposed for T2.3 do not account for marine regions or species. We provide more data directly on the other indicator mentioned (Proportion of terrestrial, freshwater, and marine ecological areas within PCAs) for marine areas in a FAIR workflow. Our workflow and indexes are useful resources that monitor Target 2 of the draft monitoring framework for the post-2020 global biodiversity framework. Additionally, the inclusion of ABNJ in the indexes is extremely important given current discussions on a new implementing agreement for the United Nations Convention on the Law of the Sea to protect marine biodiversity in areas beyond national jurisdiction and thus the whole ocean29.Table 1 Subset of the draft monitoring framework for the post-2020 global biodiversity framework available online (https://www.cbd.int/sbstta/sbstta-24/post2020-monitoring-en.pdf).Full size tableThe GPHPI is a valuable index that reveals the protection status of habitats distributed globally. The index highlights that not all countries have the same amount of habitat, and international effort is needed to conserve biodiversity worldwide, aspects that the LPHPI does not readily show. It is valuable to understand where habitats are covered by protected areas and where further efforts need to be placed. For example, Norway has a relatively low LPHPI (0.168) and simultaneously a relatively high GPHPI (top 11%) because of the total area of mapped habitats within their jurisdiction and their efforts to conserve them. If they can improve their LPHPI to 0.3 (30%), their GPHPI would also increase since they have a large area of habitats. But even with less than 30% of these habitats in PCAs, the protection Norway has established, or other countries have in a similar situation, substantially contributes to the global effort.Jurisdictions have direct control over their LPHPI. Increasing the protected area coverage of their marine and coastal habitats will directly increase the index score. Small countries and territories with a limited area may see large improvements in their LPHPI through a few additional protected areas, while their GPHPI score will not increase much from this effort. For these jurisdictions, international strategies need to be implemented to promote the conservation of marine and coastal habitats. The GPHPI also reveals that each jurisdiction may physically contribute only a small percentage. However, when combined, these could provide the overall coverage of PCAs distributed around the world that is ecologically advisable to promote overall biodiversity.Within the targeted analysis of the global proportion of habitats protected, any jurisdiction that protects more than 30% of its habitat extent can move from a negative to a positive score; thus, it is relative to each jurisdiction. However, the targeted analysis also reflects the absolute contribution of each jurisdiction. In particular, the targeted analysis can be interpreted to reveal jurisdictions that have the highest opportunity to conserve the most habitat, if they can reach the 30% target. Thus, this informs part of goal D of the post-2020 biodiversity framework, which requires understanding where to prioritize effort. The jurisdictions that rank the lowest in the analysis, currently ABNJ, Norway, Papua New Guinea, Nigeria, and Iraq (Fig. 4), represent a great opportunity to further expand PCAs to 30% coverage of marine habitats within their territorial waters and coast, as these would contribute the most added area. The jurisdictions that score highest have the opportunity to monitor and improve the effectiveness of their PCAs to adequately protect these marine habitats and reduce surrounding pressures, especially since they contribute significantly to the total global extent of these habitats.LimitationsOne limitation of our indexes is that they do not distinguish between areas that are readily protected (e.g., due to remoteness) and those that most urgently need protection (e.g., highly threatened biodiverse locations)30,31. Additionally, the analysis presented here is sensitive to the choice of coastal and marine habitats included in the indexes. We selected these six habitats based on the availability of high-quality spatially explicit global data recognized by the scientific community. Each habitat dataset is published in a peer-reviewed journal and available online (https://data.unep-wcmc.org/datasets) within the UN Environment Programme World Conservation Monitoring Centre (UNEP-WCMC) website and follows their data standards. The data represent the known and mapped distribution of habitats; thus, there are inherent knowledge gaps between the actual extent and available data. For example, it is likely that significant portions of cold-water corals, particularly in the ABNJ, are still unknown. Over time, the workflow will be updated and improved yearly to strengthen data coverage, and if additional high-quality data on habitats emerge, these will be included ensuring the indexes stay up to date and relevant. The original analysis with the same habitats will also be repeated to ensure a consistent time series of the indexes is provided.An important consideration when using these indexes is that habitat extent that spatially aligns with a PCA does not necessarily mean that a particular habitat is protected. For example, some PCAs enforce regulations on the water area (e.g., fishing exclusion), but do not prevent mangrove deforestation. Additionally, because of the buffering of points within the workflow, some of the habitats that are counted as protected may fall near a PCA but not within it. Nevertheless, our analysis assumes that habitats that fall within a PCA will be better conserved than habitats not within a PCA, as the primary purpose of protected areas is conservation. Similarly, we assume that other effective area-based conservation measures provide some conservation benefit and are often sustainably managed by local communities and indigenous peoples who live on them32,33.The LPHPI and GPHPI indexes report detailed information for policymakers, the scientific community, and stakeholders to understand the state of protection for marine and coastal habitats at both global and local levels. Simple metrics like these indexes that the public and politicians understand help communicate the plight of ocean health and efforts to improve it. The workflow, based on open-source programming and datasets, is reproducible and scalable and was developed to allow other scientists and data providers to calculate the indexes for any areas or habitats of interest and repeat and adapt our analysis for any target. The indexes will be updated annually to ensure continued relevance and the provision of a time series to track how the world is advancing towards the goals defined by global policy, such as aspects of the Sustainable Development Goal 14, therefore bringing to the forefront the importance and status of conserving critical marine and coastal habitats. Ultimately, transparency in protection efforts, effectiveness, and representation must be improved so policymakers can grasp the current conditions, possible scenarios, and make informed decisions to meet international policy commitments34. More

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    Urban conservation gardening in the decade of restoration

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