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Predictive Allometry for Pollinating Insects 1 Running Title bioRxiv preprint doi: https://doi.org/10.1101/397604; this version posted August 22, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 Title: Pollinator size and its consequences: Predictive allometry for pollinating insects 2 Running title: Allometric scaling of pollinating insects 3 Word count: 7412 4 5 Liam K. Kendall1,2*, Romina Rader1, Vesna Gagic2, Daniel P. Cariveau3, Matthias Albrecht4, 6 Katherine C. R. Baldock5, Breno M. Freitas6, Mark Hall1, Andrea Holzschuh7, Francisco P. 7 Molina12, Joanne M. Morten5, Janaely S. Pereira6, Zachary M. Portman3, Stuart P. M. Roberts8, 8 Juanita Rodriguez9, Laura Russo10, Louis Sutter4, Nicolas J. Vereecken11 and Ignasi 9 Bartomeus12 10 11 1. School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia 12 2. CSIRO Agriculture, GPO Box 2583, Brisbane, QLD 4001, Australia 13 3. Department of Entomology, University of Minnesota, St. Paul, MN, USA 14 4. Agroscope, Agroecology and Environment, CH-8046 Zürich, Switzerland 15 5. School of Biological Sciences & Cabot Institute, University of Bristol, Bristol, BS8 1TQ, UK 16 6. Departamento de Zootecnia – CCA, Universidade Federal do Ceará, 60.356-000, Fortaleza, CE, Brazil 17 7. Animal Ecology and Tropical Biology, Biocenter, University of Würzburg, 97074 Würzburg, Germany 18 8. Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, The University of Reading, 19 Reading, RG6 6AR UK 20 9. Australian National Insect Collection, CSIRO, Canberra, ACT 2601, Australia 21 10. Botany Department, Trinity College Dublin, Ireland 22 11. Agroecology Lab,11 Interfaculty School of Bioengineers. Université Libre de Bruxelles, Boulevard du Triomphe CP 264/2, 23 B-1050 Bruxelles, Belgium 24 12. Dpto. Ecología Integrativa, Estación Biológica de Doñana (EBD-CSIC), 41092 Sevilla, Spain 25 26 *Corresponding author: L. K. Kendall, Email: [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/397604; this version posted August 22, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 27 Abstract 28 1. Body size is an integral functional trait that underlies pollination-related ecological 29 processes, yet it is often impractical to measure directly. Allometric scaling laws have 30 been used to overcome this problem. However, most existing models rely upon small 31 sample sizes, geographically restricted sampling and have limited applicability for 32 non-bee taxa. Predictive allometric models that consider biogeography, phylogenetic 33 relatedness and intraspecific variation are urgently required to ensure greater 34 accuracy. 35 2. Here, we measured body size, as dry weight, and intertegular distance (ITD) of 391 36 bee species (4035 specimens) and 103 hoverfly species (399 specimens) across four 37 biogeographic regions: Australia, Europe, North America and South America. We 38 updated existing models within a Bayesian mixed-model framework to test the power 39 of ITD to predict interspecific variation in pollinator dry weight in interaction with 40 different co-variates: phylogeny or taxonomy, sexual dimorphism and biogeographic 41 region. In addition, we used ordinary least squares (OLS) regression to assess 42 intraspecific dry weight – ITD relationships for 10 bee and five hoverfly species. 43 3. Including co-variates led to more robust interspecific body size predictions for both 44 bees (Bayesian R2: 0.946; ΔR2 0.047) and hoverflies (Bayesian R2: 0.821; ΔR2 0.058) 45 relative to models with ITD alone. In contrast, at the intraspecific level, our results 46 demonstrate that ITD is an inconsistent predictor of body size for bees (R2: 0.02 – 47 0.66) and hoverflies (R2: -0.11 – 0.44). 48 4. Therefore, predictive allometry is more suitable for interspecific comparative analyses 49 than assessing intraspecific variation. Collectively, these models form the basis of the 50 dynamic R package, 'pollimetry’, which provides a comprehensive resource for 51 allometric research concerning insect pollinators worldwide. 2 bioRxiv preprint doi: https://doi.org/10.1101/397604; this version posted August 22, 2018. 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. 52 53 Keywords: Apoidea, biogeography, body size, dry weight, pollimetry, pollination, R package, 54 Syrphidae 55 56 Introduction 57 Body size is an important functional trait that influences ecological patterns across all levels of 58 biological organisation. In insects, adult body size variation is the outcome of natural selection 59 affecting physiological and biochemical processes during ontogeny (Chown & Gaston 2010). 60 For example, body size impacts metabolic and growth rates (Angilletta et al. 2004; Ehnes et al. 61 2011), life history (e.g. life span and reproductive rate; Speakman 2005; Teder et al. 2008) and 62 ecological attributes, such as species abundance, trophic interactions, geographic range size 63 and dispersal ability (Brown et al. 2004; White et al. 2007; Stevens et al. 2012; Velghe & 64 Gregory-Eaves 2013; DeLong et al. 2015). In addition, body size can drive key ecosystem 65 functions and services such as decomposition, carbon cycling, predation, primary productivity 66 and pollination (Woodward & Hildrew 2002; Greenleaf et al. 2007; Rudolf & Rasmussen 2013; 67 Garibaldi et al. 2015; Schramski et al. 2015). 68 69 Body size is most commonly measured as specimen dry weight. As such, obtaining direct 70 measurements can be impractical and time consuming. Direct measurements often require 71 destructive methods, which is unfavourable for museum specimens and threatened species 72 (Rogers et al. 1977; Henschel & Seely 1997). Additionally, species with poor life-history 73 information, such as rare species with few specimens, may lead to inaccurate measurements of 74 intraspecific variation. Allometric scaling laws can be used to overcome these problems. These 75 laws refer to how traits, which can be morphological, physiological or chemical, co-vary with 76 an organism’s body size, often with important ecological and evolutionary implications (Gould 3 bioRxiv preprint doi: https://doi.org/10.1101/397604; this version posted August 22, 2018. 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. 77 1966). When these scaling laws are utilised to estimate body size or a hypothesised allometric 78 characteristic indirectly using a co-varying morphological trait, therefore circumventing the 79 use of destructive and/or time-consuming methods, we define this as ‘predictive allometry’. 80 81 Predictive allometry has emerged across many biological disciplines. The most commonly used 82 co-varying trait used to predict body size is body length, which has been used extensively in 83 fish (e.g. Karachle & Stergiou 2012), mammals (e.g. Trites & Pauly 1998) and both aquatic 84 (e.g. Burgherr & Meyer 1997) and terrestrial invertebrates (e.g. Rogers et al. 1977; Sabo et al. 85 2002). These models often show considerable predictive power (R2 > 0.9), which has led to the 86 proliferation of multiple models for a wide range of taxa (e.g. there are 26 body length – body 87 size models for Diptera – See Supporting Information). However, when compared, these 88 models show considerably different allometric scaling coefficients both within- and between 89 insect orders (Schoener 1980; Sample et al. 1993; Ganihar 1997; Brady & Noske 2006). 90 Previously, these differences have been attributed to biogeographic factors, such as latitude 91 (Martin et al. 2014) and/or methodological influences such as sampling biases (e.g. the range 92 of sampled body sizes, Sage 1982). Importantly, they have also notably failed to incorporate 93 sexual size dimorphism which is common in invertebrates (Shreeves & Field 2008). 94 95 The allometry of functional traits have been shown to influence plant-pollinator interactions, 96 specifically in bees. For example, smaller body size can be associated with preferential activity 97 periods related to available light (Streinzer et al. 2016), whereas larger body size is associated 98 with greater pollen load capacity (e.g. within Melipona quadrifasciata colonies, see Ramalho 99 et al. 1998) as well as greater interspecific foraging distances (e.g. Greenleaf et al. 2007). 100 Importantly, body size can both influence and constrain plant-pollinator interactions and trait 101 matching both within and between pollinator groups (Stang et al. 2009; Bartomeus et al. 2016). 4 bioRxiv preprint doi: https://doi.org/10.1101/397604; this version posted August 22, 2018. 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. 102 Therefore, allometric traits central to pollination-related ecological processes both appear and 103 interact at the intra- and interspecific levels. Despite their ubiquity, few predictive models for 104 body size exist for pollinating insects below the ordinal level, with one notable exception. Cane 105 (1987) pioneered a predictive model for bee body size as a function of the intertegular distance 106 (ITD) (the distance between the wing-attachment points on either side of the thorax (See Fig. 107 S1). Importantly, Cane’s allometric model identified the ITD as an important body size proxy 108 and has since been used to establish other ecologically important allometric relationships, 109 primarily at the interspecific level (e.g.
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