Mangroves Are an Overlooked Hotspot of Insect Diversity Despite Low Plant Diversity

bioRxiv preprint doi: https://doi.org/10.1101/2020.12.17.423191; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Mangroves are an overlooked hotspot of insect diversity despite low plant diversity 2 3 Darren Yeo1, Amrita Srivathsan1, Jayanthi Puniamoorthy1, Foo Maosheng2, Patrick 4 Grootaert3, Lena Chan4, Benoit Guénard5, Claas Damken6, Rodzay A. Wahab6, Ang 5 Yuchen2, Rudolf Meier1 6 7 8 1Department of Biological Sciences, National University of Singapore, 14 Science 8 Drive 4, 9 Singapore 117543 10 2Lee Kong Chian Natural History Museum, National University of Singapore, 2 Conservatory 11 Drive, Singapore 117377 12 3Royal Belgian Institute of Natural Sciences, Brussels, Belgium and National Biodiversity 13 Centre, National Parks Board, Singapore 14 4International Biodiversity Conservation Division, National Parks Board, 1 Cluny Road, 15 259569 Singapore 16 5School of Biological Sciences, The University of Hong Kong, Kadoorie Biological Sciences 17 Building, Pok Fu Lam Road, Hong Kong, SAR, China 18 6Institute for Biodiversity and Environmental Research, Universiti Brunei Darussalam, Jalan 19 Universiti, BE1410, Brunei Darussalam 20 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.17.423191; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 21 Abstract 22 We here compare the tropical arthropod fauna across a freshwater swamp and six different 23 forest types (rain-, swamp, dry-coastal, urban, freshwater swamp, mangroves) based on 24 140,000 barcoded specimens belonging to ca. 8,500 species. Surprisingly, we find that 25 mangroves, a globally imperiled habitat that had been expected to be species-poor for 26 insects, are an overlooked hotspot for insect diversity despite having low plant diversity. Our 27 study reveals a species-rich mangrove insect fauna (>3,000 species) that is distinct (>50% 28 of species are mangrove-specific), and has high species turnover across Southeast and 29 East Asia. For most habitats, plant diversity is a good predictor for insect diversity, but 30 mangroves are an exception and compensate for a comparatively low number of 31 phytophagous and fungivorous insect species by supporting an unusually rich community of 32 predators whose larvae feed in the productive mudflats. For the remaining tropical habitats, 33 the insect communities have diversity patterns that are largely congruent across guilds. The 34 discovery of such a sizeable and distinct insect fauna in a globally threatened habitat 35 underlines how little is known about global insect biodiversity. 36 Keywords 37 Insect biodiversity, Mangroves, NGS barcoding, species discovery, beta-diversity, global 38 insect decline, Southeast Asia 39 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.17.423191; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 40 Introduction 41 Insects are currently experiencing anthropogenic biodiversity meltdowns with 42 declines having attracted much attention [1–4] and controversy [5–10]. The controversy is 43 largely due to the paucity of high-quality, quantitative data with sufficient taxonomic 44 resolution for arthropods. The same paucity is also responsible for imprecise estimates of 45 global animal species richness [11, 12] and the poor understanding of geographic and 46 temporal species turnovers [13–15]. These knowledge gaps are likely to threaten the health 47 of whole ecosystems given that arthropods provide important ecosystem services [3, 16–19], 48 contribute much of the terrestrial animal biomass (~10%) [20] and are yet frequently ignored 49 in habitat assessments. The lack of baseline data is particularly worrisome at a time when 50 tropical ecosystems are heavily impacted by habitat conversion and global change [21]. 51 The situation is particularly dire for the species-rich tropics, for which few 52 comprehensive surveys have been conducted [22–24]. For example, only three of 73 studies 53 in a recent review of insect declines involved tropical sites [8]. Furthermore, tropical insect 54 surveys have traditionally focused on rainforests [24], with other habitats being largely 55 neglected. Mangrove forests are a prime example of a tropical habitat for which the insect 56 fauna is poorly characterized. Mangroves used to cover more than 200,000 km2 of the global 57 coastline [25], but have been experiencing an annual area loss of 1-2% [25, 26]. Indeed, the 58 losses of mangroves far exceed those of more high-profile ecosystems such as rainforests 59 and coral reefs [26]. Unfortunately, these losses are further exacerbated by climate change 60 [27], with some simulations predicting a further reduction by 46–59% for all global coastal 61 wetlands by the year 2100 [28]. This is particularly worrying as mangrove ecosystems 62 sequestrate a particularly large amoung of carbon per hectare [29]. These changes will not 63 only endanger entire ecosystems that provide essential ecosystem services [30–32], but 64 also threaten the survival of numerous mangrove species with unique adaptations. 65 Mangrove specialists with such adaptations are well known for vertebrates and vascular 66 plants [33, 34], but the invertebrate diversity is poorly known. 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.17.423191; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 67 One reason why the mangrove insect fauna may have have received little attention is 68 low plant diversity. Tropical arthropod diversity is usually positively correlated with plant 69 diversity [23, 24, 35] which suggested that mangroves would not be species-rich for insects 70 and provide few insights into one of the key questions in insect biodiversity, viz. 71 understanding whether insect herbivores drive high plant diversity in the tropics [36–38] or 72 vice versa [22, 39]. Arguably, the traditional focus on this question may have had the 73 undesirable side-effect that the insect fauna of habitats with low plant diversity received little 74 interest. Yet, many of these habitats are threatened with destruction. The few existing 75 studies of mangrove insects focused on specific taxa [40–42], only identified specimens to 76 higher taxonomic levels [43–45], and/or lacked quantitative comparison with the insect fauna 77 of adjacent habitats. Given these shortcomings, it may not surprise that these studies 78 yielded conflicting results [44, 46, 47] with some arguing that high salinity and/or low plant 79 diversity [33, 44, 46] were responsible for a comparatively poor insect fauna, while others 80 reporting high levels of species diversity and specialization [47]. 81 Here, we present the results of a comprehensive study of species richness and 82 turnover of arthropods across multiple tropical habitats. The assessment is based 83 on >140,000 barcoded specimens obtained over >4 years from mangroves, rainforests, 84 swamp forests, disturbed secondary urban forests, dry coastal forests, and freshwater 85 swamps in Singapore (Fig. S1). In addition, we assess the species richness and turnover of 86 mangrove insects across East and Southeast Asia by including samples from Brunei, 87 Thailand, and Hong Kong. Specifically, our study (1) estimates mangrove insect diversity, (2) 88 evaluates the distinctness in reference to five different forest habitats, (3) analyzes the 89 biodiversity patterns by ecological guild, and (4) determines species turnover across larger 90 geographic scales. Most of the work was carried out in Singapore because it has a large 91 variety of different habitats that occur within 40km on a small island (724 km2) that lacks 92 major physical barriers. In addition, all habitats have experienced similar levels of habitat 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.17.423191; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 93 degradation or loss (>95% overall loss of original vegetation cover [48]; ca. 90% loss of 94 rainforest [49]; ca. 93% loss of swamp forest [50]; 91% loss for mangroves [51]). 95 A thorough assessment of insect biodiversity requires dense sampling over an 96 extended period of time [52–54]. We sampled 107 sites in Singapore using Malaise traps. All 97 samples were subsequently sorted to 13 arthropod orders (Table S2) with Diptera and 98 Hymenoptera contributing the largest number of specimens (>75%: Table S2, see Fig. S2 99 for species composition). Given the large number of specimens collected, we only barcoded 100 subsets that represented different taxa and ecological guild

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