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Optimal restoration for pollination services increases forest cover while doubling agricultural profits [1]

['Sofía López-Cubillos', 'School Of Earth', 'Environmental Science', 'Centre For Biodiversity', 'Conservation Science', 'University Of Queensland', 'St Lucia', 'Brisbane', 'Queensland', 'School Of Geography']

Date: 2023-05

Abstract Pollinators are currently facing dramatic declines in abundance and richness across the globe. This can have profound impacts on agriculture, as 75% of globally common food crops benefit from pollination services. As many native bee species require natural areas for nesting, restoration efforts within croplands may be beneficial to support pollinators and enhance agricultural yields. Yet, restoration can be challenging to implement due to large upfront costs and the removal of land from production. Designing sustainable landscapes will require planning approaches that include the complex spatiotemporal dynamics of pollination services flowing from (restored) vegetation into crops. We present a novel planning framework to determine the best spatial arrangement for restoration in agricultural landscapes while accounting for yield improvements over 40 years following restoration. We explored a range of production and conservation goals using a coffee production landscape in Costa Rica as a case study. Our results show that strategic restoration can increase forest cover by approximately 20% while doubling collective landholder profits over 40 years, even when accounting for land taken out of production. We show that restoration can provide immense economic benefits in the long run, which may be pivotal to motivating local landholders to undertake conservation endeavours in pollinator-dependent croplands.

Citation: López-Cubillos S, McDonald-Madden E, Mayfield MM, Runting RK (2023) Optimal restoration for pollination services increases forest cover while doubling agricultural profits. PLoS Biol 21(5): e3002107. https://doi.org/10.1371/journal.pbio.3002107 Academic Editor: Pedro Jordano, Estacion Biologica de Doñana CSIC, SPAIN Received: September 12, 2022; Accepted: April 4, 2023; Published: May 23, 2023 Copyright: © 2023 López-Cubillos et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the paper and its Supporting Information files. Funding: SLC was supported by a Colombian Ministry of Education grant (COLCIENCIAS, No. 728) and the Research Training program provided by the Graduate School from the University of Queensland. RKR is funded by an Australian Research Council DECRA Fellowship (DE210100492). EMM is supported by an Australian Research Council Future Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction To address the global biodiversity crisis, landscape restoration has gained increasing traction [1], leading to initiatives such as the “Bonn challenge,” which aims to restore 350 million hectares of land [2], and the United Nations’ declare 2020–2030 as the “Decade on Ecosystem Restoration.” At the same time, food demand is expected to increase by 50% to 70% by 2050 [3], potentially expanding agricultural land use and threatening biodiversity [4] along with crucial ecosystem services [5]. Therefore, restoration can be perceived as both as a competing activity with agricultural land use and crop production [6,7] and as an action than can cost effectively protect biodiversity and increase agricultural outcomes through the flow of ecosystem services critical to agriculture, such as pollination [8]. Pollination is a significantly important service in agricultural landscapes as 75% of agricultural crops benefit from it [9]. Studies have quantified that the restoration of native flora adjacent to some berry crops [10] resulted in yield increases of 5% to 6% [11,12] and by 1.5 kg per tree for all mango cultivars growing near wild flowering areas [13]. However, whether these increased yields can compensate for the costs of setting aside restored lands at a landscape scale remains unclear. In addition, not all biodiversity nor the ecosystem services it provides is realised immediately after initial restoration activities, a reality that represents a hurdle to the widespread uptake of restoration measures in agricultural landscapes [14]. For example, restoration efforts near tea, shade coffee, cardamom, and eucalyptus plantations took 9 to 17 years to see increased bird abundance in active restoration sites [15]. Further, restoration incurs upfront and ongoing financial costs can be substantial to ensure restoration success [16]. Therefore, understanding how restoration provides financial benefits over time via ecosystem services to agriculture is also essential. A good example is the increased profitability after 3 to 5 years following restoration near blueberry fields due to the benefits from pollination services [11]. As pollination is a key service to many crops, it is therefore important to quantify the bee abundance and the economic benefits from different restored patches with a range of restoration ages across the landscape. Ultimately, the question remains, where and how much land can be restored for biodiversity conservation over time, without resulting in declines in agricultural profits? Spatial optimization is a modelling approach that allows a quantitative analysis of the trade-offs between conservation and agriculture production using ecosystem services [17]. Furthermore, Kennedy and colleagues [18] and López-Cubillos and colleagues [19] have found that explicitly accounting for ecosystem services in spatial optimization under different scenarios reveals positive net social and environmental benefits by increasing income or social equity. Previous studies have explored the economic importance of restored lands to crop pollination [11], including using spatial optimization tools [20–22]. However, no studies, to our knowledge, have simultaneously considered demand for pollination services at a landscape scale (rather than at a farm scale as done by Blaauw and Isaacs [11]) and the changes for pollinator abundance with the services they provide in a dynamic temporal manner over a specific timeframe, including the economic returns they deliver. We used coffee as a case study given its importance as a cash crop in the Global South [23] and because it is known to benefit from pollination provided by wild bees [24–27]. Indeed, while coffee can self-pollinate, the yields of Coffea arabica in particular can increase from 10% to 30% due to bee pollination [25,26]. The specific system we used was coffee in Tarrazú, one of the main coffee producing canton (administrative division) in Costa Rica. Coffee production in this region has been shown to decrease by 18% when crops are too far from forest [28,29]. Using this system, we answer the following questions: (1) To what extent can the strategic allocation of land for restoration achieve both conservation and crop production goals? (2) How do these benefits change over time? (3) How important is agricultural expansion to these outcomes?

Discussion We found that strategic planning can capture the benefits of restoration to agricultural production through pollination services, which can lead to substantial economic benefits: up to a doubling of agricultural profits (NPV), even accounting for the lost production on restored lands. This is contrary to previous work that assessed the economic benefits 50 years post initial restoration that showed that while nonmarket ecosystem services (e.g., cultural, aesthetic, and recreational value) were improved, economic benefits were not achieved in marketed ecosystem services (e.g., carbon markets) [68]. However, this previous work did not consider the ecosystem services to agriculture, such as pollination, which we have shown are crucial in delivering economic benefits. Our results showed an increase in both forest cover and profit for most of the goals (i.e., “balanced” and “profit focused”) relative to baseline levels. We have even demonstrated improvements for profit and forest cover in the balanced goal when we allow coffee expansion and restoration at the same time. This highlights that strategically prioritising restoration not only provides biodiversity benefits but also enhances local livelihoods in the tropics [69]. The spatial arrangement of our “balanced” and “profit-focused” goals contained both large contiguous areas of forest and small forest patches within coffee. This suggests a mix of land sharing (many small fragmented forest patches) and land sparing (large areas set aside) is optimal in these landscapes, which is in line with other studies for the conservation of remanent forest in coffee landscapes [17]. Our results appear to differ from previous studies that showed that sparing is better in agricultural landscapes [70]. A result that may be explained by our focus on ecosystem service flows rather than a species focus (e.g., bird and plant biodiversity). Furthermore, pollination services operate over small spatial scales [71] and they also depend on animal movement from forest fragments, the interspersion of remnant or restored forest within croplands is akin to a land sharing approach [72]. However, our findings are in line with emerging literature showing that mixed sharing/sparing landscapes are optimal when we capture the spatial heterogeneity of landscapes, with a mix of remanent forest, restored areas, and agricultural lands [73]. In development frontiers, where further crop expansion may be unavoidable, positive results for biodiversity can still be achieved, despite the loss of some remnant forest. The “balanced” goal increased the total amount of the forest index by 15% and increased agricultural profit by 109% compared to the baseline. However, this is far from a green light for unchecked agricultural development, as our results were only achieved by strategically allocating new coffee production across landscapes, while retaining substantial forest patches. Caution is thus needed with crop expansion, as removing nature to increase economic gains will reduce the resiliency of the ecosystem and increase environmental variability (e.g., longer droughts) and potentially lead to ecosystem collapses if not managed in line with our understanding of the ecology of fragmented landscapes [74]. Furthermore, some landscapes with dense forest cover (≥75% canopy) that are located nearby coffee crops (approximately 1 km) have higher pollination richness and fruit set due to pollination services [24]; therefore, focusing only on restoration rather than deforestation and restoration at the same time would be the best strategy. Our results show the potential for how restoring lands in agricultural landscapes can achieve environmental conservation outcomes without being an economic burden in the long term. Accurately calculating the economic benefits from pollination services can be challenging as costs and benefits flow at different times, and multiple key variables can affect the outcome [64]. In this case study, our results were robust to variation in these key variables—positive outcomes for agricultural profits and net forest area relative to the baseline were achieved in most cases. Varying the discount rate used to calculate NPV had the biggest impact on results and as such, it is a factor that must be contemplated carefully when using these rates to plan restoration activities over time [75,76]. Specifically, higher discount rates reduce the contribution of future economic benefits and costs to the NPV calculation and are therefore likely to favour agricultural production (with immediate benefits) over restoration (with a slower accrual of benefits). Alternatively, reducing the cost of restoration by 25% increases the area of forest restored by up to 6% for the “profit focused” goal when only considering restoration. Such cost reductions could be achieved by using a mix of passive [77] and active restoration approaches. However, as benefits may be slower to accumulate with passive restoration, this remains an important area for further research. Our model assumes that bee abundance will fully recover after 40 years in tropical forest and that the pollination benefit from restoration will be achieved between 6 to 15 years of being restored, as substantial pollination benefits are provided by common species, such as Apis mellifera [29]. These timelines are estimates for our case study system and should not be used as general assumptions that can be applied to other systems. The literature about the benefits of restoration on bee abundance is mixed, with some studies aligning with our assumptions and others unaligned. It is much better to set these timelines according to the known understanding of each landscape and forest system to which our method is applied and even then, care should be taken to acknowledge that recovery times can and do vary extensively within and across systems. Positive results for bees’ population recovery after small-scale restoration approaches (such as hedgerow restoration) have been found in intensive agricultural landscapes after 7 to 10 years of restoration [54,55,78]. In restored sections of riparian forest, however, Gutiérrez-Chacón and colleagues [79] and Williams and colleagues [80] found that bee communities are not similar to reference riparian areas or forests. Gutiérrez-Chacón and colleagues [79] highlighted that species composition showed progress in recovery in this system and suggested more time (>13 years) would be needed in addition to better management actions, such as fencing to protect habitat from cattle, to see a return to a species composition similar to reference sites. We found that even when the sole goal of restoration was to maximise profit, it was still optimal to restore forest patches throughout the coffee landscape, solidifying the importance of pollination to production. However, economic benefits from restoration take time to materialise; for example, the “balanced” goal for the “expansion and restoration” context took considerable time to achieve the highest profitability when we allow restoration and forest expansion at the same time. Therefore, understanding these temporal differences in profitability can help to identify leverage points to enhance the uptake of restoration. Payment for ecosystem services (PES) schemes could compensate landholders for the initial restoration actions, which would help address this temporal mismatch in economic costs and benefits [81–83]. Indeed, these types of schemes have been successful in other tropical agricultural lands where farmers receive financial incentives in line with the profits they would have received if they would have continued agricultural production (i.e., opportunity costs [84]). Our restoration solutions could feasibly involve multiple landholders in restoration efforts, some of which are likely to be smallholders (as is very common in Costa Rica [85]). The inclusion of many small landholders could represent a challenge for implementing a PES scheme, as this can increase transaction costs and reduce the potential for coordinated landscape management. If the transaction cost exceeds, or is close to, the PES incentive payment, the project may not be viable [86]. In such cases, farmer collectives may form an avenue to reduce transaction costs and maintain the benefits of these payment schemes [81,85]. In addition, more extensive and ongoing PES may be required to incentivise the restoration of the larger forest patches—meaning greater conservation benefits as seen in our “conservation” and “balanced” goals—as they show larger trade-offs with profitability. Strategic planning for restoration is vital, especially in the global south, which contains many biodiversity hotspots alongside important regions for agricultural development and community livelihoods [82,87]. Therefore, restoration should be planned in a manner that minimises the impacts on food production and where farmers can benefit from ecosystem services [88]. Unfortunately, despite the importance of pollination services, their inclusion in land-use plans and policymaking is usually ignored or poorly implemented [89,90]. Our spatial framework is a step towards reconciling the often-divergent objectives of nature restoration and agricultural production by including pollination services. We found that the strategic allocation of restored habitat within croplands can synergistically enhance biodiversity and agricultural production, and that some level of restoration is ideal even if solely aiming to maximise profit. This is relevant to many landscapes across the globe with vast swaths of monoculture plantations, where strategic restoration could improve outcomes for both pollinators [91] and landholder profits. Our framework integrates the spatiotemporal dynamics inherent to ecological processes and economic information, which is a key advance to guide decision-making in agricultural landscapes around the world [92]. Landscape restoration for targeted species, like wild bees, shows that we can have potential win-wins for both biodiversity and people in heavily human-modified landscapes.

Acknowledgments We are thankful with Dr. Rebecca Chaplin-Kramer and Dr. Taylor Ricketts for making comments on early versions of the manuscript.

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