Range-wide population viability analyses reveal high sensitivity to wildflower harvesting in extreme environments

The ecological effects of harvesting from wild populations are often uncertain, especially since the sensitivity of populations to harvesting can vary across species’ geographical ranges. In the Cape Floristic Region (CFR, South Africa) biodiversity hotspot, wildflower harvesting is widespread and economically important, providing an income to many rural communities. However, with very few species studied to date, and without considering range-wide sensitivity to harvesting, there is limited information available to ensure the sustainability of wildflower harvesting.

We studied geographical variation in sensitivity to wildflower harvesting for 26 Proteaceae shrubs with fire-driven life cycles using population viability analyses. We developed stochastic, density-dependent population models that were parameterized from individual demographic rates (adult fecundity, seedling recruitment and adult fire survival) and local environmental conditions across the geographical ranges of the study species. We then simulated the effects of harvesting on populations in different environments across species ranges. Our model simulations predicted extinction risk per population, and we derived extinction probabilities over 100 years in response to different harvesting regimes. We used these population-level extinction probabilities to quantify inter- and intraspecific variation in sensitivity to wildflower harvesting, and to explore how geographical variation in sensitivity depends on environmental conditions (climate, soil fertility and fire disturbance).

We detected considerable inter- and intraspecific variation in sensitivity to wildflower harvesting for the 26 study species. This held for both ‘nonsprouters’ and ‘resprouters’ (species with low and high fire persistence ability, respectively). Intraspecific variation in sensitivity to harvesting showed varying geographical patterns and associated with environmental variation. Notably, sensitivity was high towards range edges and at the climatic extremes of species ranges, respectively.

Synthesis and applications: We show the importance of combining spatial demographic data, density-dependent population dynamics and environmental variation when assessing sensitivity to harvesting across species geographical ranges. Our findings caution against the application of general harvesting guidelines irrespective of species, geographical location or local environmental conditions. Our range-wide population viability analyses provide insights for developing species-specific, spatially nuanced guidelines for conservation management. Our approach also identifies species and areas to prioritise for monitoring to prevent the overexploitation of harvested species.23-Mar-2021

Methods
Demographic data can be found in the cited literature of this article (notably Treurnicht et al. 2016; Pagel et al. 2020 and supporting information of these published articles). These demographic data were partly used under license agreements from provincial and national conservation organisations in South Africa (CapeNature and SANParks) and are available from the lead author ([e-mail]) upon reasonable request and with the permission of these organisations.

-Treurnicht, M., Pagel, J., Esler, K.J., Schutte‐Vlok, A., Nottebrock, H., Kraaij, T. et al. (2016) Environmental drivers of demographic variation across the global geographical range of 26 plant species. Journal of Ecology, 104, 331–342.

-Pagel, J., Treurnicht, M., Bond, W.J., Kraaij, T., Nottebrock, H., Schutte-Vlok, A., Tonnabel, J., Esler, K.J. & Schurr, F.M. (2020) Mismatches between demographic niches and geographic distributions are strongest in poorly dispersed and highly persistent plant species. Proceedings of the National Academy of Sciences 117, 3663-3669.

Environmental data are from various sources cited in the main text of this article (Treurnicht et al. 2021) and include:

- Schulze, R.E. (2007) South African Atlas of Climatology and Agrohydrology, Technical Report 1489/1/06. Water Research Commission, Pretoria, South Africa.

- Wilson, A.M., Latimer, A.M. & Silander, J.A. (2015) Climatic controls on ecosystem resilience: postfire regeneration in the Cape Floristic Region of South Africa. Proceedings of the National Academy of Sciences of the USA, 112, 9058–9063.

野生种群收获的生态效应通常难以确定，尤其是种群对收获的敏感性会随物种的地理分布范围发生变化。在南非开普植物区系（Cape Floristic Region, CFR）这一生物多样性热点区域，野生花卉采集活动十分普遍且具有重要经济价值，为众多乡村社区提供了收入来源。然而，截至目前仅对极少数物种开展了相关研究，且未考虑物种全分布区对收获的敏感性，因此可用于保障野生花卉采集可持续性的有效信息十分有限。

我们针对26种具有火驱动生活史的山龙眼科（Proteaceae）灌木，采用种群生存力分析（Population Viability Analysis, PVA）方法研究了其对野生花卉收获的敏感性的地理变异。我们构建了随机密度依赖种群模型，模型参数来自个体种群统计率（成虫繁殖力、幼苗更新量和成体火灾存活率）以及研究物种地理分布范围内的局域环境条件。随后我们模拟了物种分布区内不同环境下的种群收获效应。模型模拟结果预测了各种群的灭绝风险，并推导了100年时间尺度下不同收获模式对应的灭绝概率。我们利用这些种群水平的灭绝概率，量化了野生花卉收获敏感性的种间与种内变异，并探索了敏感性的地理变异如何受环境条件（气候、土壤肥力与火灾干扰）影响。

我们在26种研究物种中检测到了显著的种间和种内收获敏感性变异，这一规律在“非萌芽种”和“萌芽种”（分别对应火灾存续能力较低和较高的物种）中均成立。种内收获敏感性变异呈现出多样的地理格局，并与环境变异相关。值得注意的是，敏感性在分布区边缘以及物种分布的气候极端区域分别较高。

综合与应用：我们证实，在评估物种地理分布范围内的收获敏感性时，结合空间种群统计数据、密度依赖种群动态与环境变异至关重要。本研究结果警示，不应无视物种、地理位置或局域环境条件而套用统一的收获指南。我们开展的全分布区种群生存力分析，可为制定物种特异性、空间精细化的保护管理指南提供参考。本研究方法还可识别需要优先开展监测的物种与区域，以防止收获物种被过度开发。2021年3月23日

方法
种群统计数据可参见本文引用的文献（特别是Treurnicht等，2016年；Pagel等，2020年，以及上述两篇发表文章的补充材料）。这些种群统计数据的部分使用已获得南非省级和国家保护机构——开普自然保护局（CapeNature）与南非国家公园（SANParks）的许可协议授权。如需获取相关数据，可联系通讯作者（[e-mail]），但需获得上述机构的许可。

-Treurnicht, M., Pagel, J., Esler, K.J., Schutte‐Vlok, A., Nottebrock, H., Kraaij, T. 等. (2016) 26种植物全球地理分布范围内种群变异的环境驱动因子. 《Journal of Ecology》, 104卷, 331–342页.

-Pagel, J., Treurnicht, M., Bond, W.J., Kraaij, T., Nottebrock, H., Schutte-Vlok, A., Tonnabel, J., Esler, K.J. & Schurr, F.M. (2020) 种群统计生态位与地理分布的错配在扩散能力弱、存续能力强的植物物种中最为显著. 《美国国家科学院院刊》(Proceedings of the National Academy of Sciences, PNAS), 117卷, 3663–3669页.

环境数据来自本文正文中引用的多种来源（Treurnicht等，2021年），包括：
- Schulze, R.E. (2007) 《南非气候学与农业水文学图集》，技术报告1489/1/06，南非水研究委员会，比勒陀利亚。
- Wilson, A.M., Latimer, A.M. & Silander, J.A. (2015) 气候对生态系统恢复力的控制：南非开普植物区系的火灾后更新. 《美国国家科学院院刊》(Proceedings of the National Academy of Sciences, PNAS), 112卷, 9058–9063页.