Decades of native bee biodiversity surveys at Pinnacles National Park highlight the importance of monitoring natural areas over time

RESEARCH ARTICLE Decades of native bee biodiversity surveys at Pinnacles National Park highlight the importance of monitoring natural areas over time Joan M. Meiners ID1*, Terry L. Griswold2, Olivia Messinger Carril3 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 School of Natural Resources and Environment, University of Florida, Gainesville, Florida, United States of America, 2 USDA-ARS Pollinating Insects Research Unit (PIRU), Utah State University, Logan, Utah, United States of America, 3 Independent Researcher, Santa Fe, New Mexico, United States of America * Abstract OPEN ACCESS Citation: Meiners JM, Griswold TL, Carril OM (2019) Decades of native bee biodiversity surveys at Pinnacles National Park highlight the importance of monitoring natural areas over time. PLoS ONE 14(1): e0207566. https://doi.org/10.1371/journal. pone.0207566 Editor: Kleber Del-Claro, Universidade Federal de Uberlândia, BRAZIL Received: October 31, 2018 Accepted: December 17, 2018 Published: January 17, 2019 Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Data Availability Statement: All relevant data are within the manuscript and its Supporting Information files. These same data are also publicly available on GitHub at https://github.com/ beecycles/pinnacles_bee_biodiversity. Thousands of species of bees are in global decline, yet research addressing the ecology and status of these wild pollinators lags far behind work being done to address similar impacts on the managed honey bee. This knowledge gap is especially glaring in natural areas, despite knowledge that protected habitats harbor and export diverse bee communities into nearby croplands where their pollination services have been valued at over $3 billion per year. Surrounded by ranches and farmlands, Pinnacles National Park in the Inner South Coast Range of California contains intact Mediterranean chaparral shrubland. This habitat type is among the most valuable for bee biodiversity worldwide, as well as one of the most vulnerable to agricultural conversion, urbanization and climate change. Pinnacles National Park is also one of a very few locations where extensive native bee inventory efforts have been repeated over time. This park thus presents a valuable and rare opportunity to monitor long-term trends and baseline variability of native bees in natural habitats. Fifteen years after a species inventory marked Pinnacles as a biodiversity hotspot for native bees, we resurveyed these native bee communities over two flowering seasons using a systematic, plot-based design. Combining results, we report a total of 450 bee species within this 109km2 natural area of California, including 48 new species records as of 2012 and 95 species not seen since 1999. As far as we are aware, this species richness marks Pinnacles National Park as one of the most densely diverse places known for native bees. We explore patterns of bee diversity across this protected landscape, compare results to other surveyed natural areas, and highlight the need for additional repeated inventories in protected areas over time amid widespread concerns of bee declines. Funding: This project was funded by Pinnacles National Park through the Great Basin Cooperative Ecosystem Studies Unit (Task Agreement number P10AC00577 awarded to TLG). (http://www.cesu. psu.edu/unit_portals/unit_materials/cooperative_ agreements/GRBA/GRBA_CESU_2016_AMD01. PLOS ONE | https://doi.org/10.1371/journal.pone.0207566 January 17, 2019 1 / 23 Native bee biodiversity surveys highlight the importance of monitoring natural areas over time pdf). JMM was supported by a University of Florida Biodiversity Institute Graduate Fellowship, and by the Utah State University Ecology Center. (https:// biodiversity.institute.ufl.edu/; https://ecology.usu. edu/). 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 The importance of bees as critical ecosystem service providers can scarcely be exaggerated. Twenty thousand species of bees worldwide provide the pollination services required for reproduction in 85% of wild and cultivated plants [1,2]. In the United States, the economic importance of bees to agriculture has been valued at up to $14.6 billion annually [3], with $3.08 billion and up to 30% of the U.S. diet specifically credited to the four thousand North American species of native, non-honey bees [4]. Diverse assemblages of native bees have been found capable of enhancing fruit set and yield in the presence of imported honey bees, and of providing adequate pollination for a majority of crops in their absence [5–7]. In natural areas, without the manpower of imported, managed honey bee hives, native bees play a key role in maintaining plant communities that provide soil structure, shelter other invertebrate ecosystem service providers, and establish the base of the food chain [8,9]. Although native bees are often observed pollinating agricultural fields, they seldom nest there. Instead, they rely on nearby remnant patches of semi-natural habitat, a resource that is rapidly disappearing with increasing agricultural intensification, habitat fragmentation, and urban development [10–12]. Despite recognition of natural areas as valuable reservoirs of pollinators [13,14], research on native bee ecology remains concentrated in urban or agricultural settings where baselines may already reflect impacts of degraded ecosystems. Compared to massive honey bee research efforts, progress towards a holistic understanding of how to protect wild bee communities or the habitats they require has not matched their value as pollinators or the known risks they face [15–17]. The relative paucity of research on native bees is due, in part, to the complexity of their biology and behaviors, particularly in wild landscapes. Efforts to monitor wild bees must contend with the ‘axonomic impediment’ of expertise required to evaluate their vast global biodiversity, and the logistics of sampling a taxon with rapid spatiotemporal turnover, short lifespans, and solitary, elusive habits [18–21]. Unlike many taxa that follow a latitudinal biodiversity gradient [22], bee diversity is highest in xeric and Mediterranean environments, owing to strong seasonal blooms and well-drained soils—features which support a range of foraging specializations and a high temporal turnover of ground-nesting species [19,20,23]. When environmental conditions signal a poor year for host plants, some ground-nesting, specialist bee species can remain underground in diapause for additional years, necessitating multi-year biodiversity monitoring (...truncated)