Cyanobacterium) Accrual Along Velocity and Nitrate Gradients in Three New Zealand Rivers

Canadian Journal of Fisheries and Aquatic Sciences Reach and mat scale differences in Microcoleus autumnalis (cyanobacterium) accrual along velocity and nitrate gradients in three New Zealand rivers Journal: Canadian Journal of Fisheries and Aquatic Sciences Manuscript ID cjfas-2019-0133.R2 Manuscript Type: Article Date Submitted by the 13-Jul-2019 Author: Complete List of Authors: McAllister, Tara; The University of Auckland, Te Pūnaha Matatini Wood, Susanna; Cawthron Institute Mackenzie,Draft Emma; University of Canterbury Hawes, Ian; University of Waikato Keyword: Phormidium, growth rates, velocity, NUTRIENTS < General Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/cjfas-pubs Page 1 of 41 Canadian Journal of Fisheries and Aquatic Sciences 1 Reach and mat scale differences in Microcoleus autumnalis (cyanobacterium) accrual along 2 velocity and nitrate gradients in three New Zealand rivers 3 4 Tara G. McAllister 5 Susanna A. Wood 6 Emma M. MacKenzie 7 Ian Hawes 8 9 Tara McAllister- Te Pūnaha Matatini, University of Auckland, Auckland 10 ([email protected]) 11 Susanna Wood- Cawthron Institute, Private Bag 2, Nelson, New Zealand 12 ([email protected]) 13 Emma MacKenzie- Waterways Centre for Freshwater Management, University of Canterbury, 14 Christchurch, New Zealand ([email protected]) 15 Ian Hawes- Coastal Marine Field Station, University of Waikato, 58 Cross Road, Tauranga, New 16 Zealand ([email protected]) 17 18 19 Contact author: 20 Tara G. McAllister 21 Te Pūnaha Matatini, University of Auckland,Draft Address 22 Email: [email protected] 23 24 https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 2 of 41 25 Abstract 26 Proliferations of the toxic, mat-forming cyanobacterium Microcoleus autumnalis are an 27 increasingly recognized problem in cobble bed rivers worldwide. This study explored how 28 flow and nutrient concentrations influence mat expansion. M. autumnalis was inoculated into 29 cobbles placed in runs, riffles and pools in three rivers with different nutrient conditions and 30 mat size was monitored over 21 days. The following hypotheses were tested: (1) mat 31 expansion will reflect cover increases at the reach scale; (2) biomass and cover will be 32 highest in high velocity habitats; and (3) under similar velocities, nutrient concentrations will 33 be more important than other abiotic and biotic variables in determining expansion rates. Mat 34 expansion accurately reflected the increase in reach-scale cover, and expansion was most 35 rapid at intermediate water velocities (0.25–0.45 m s-1). Mats persisted the longest in riffles. 36 Accrual cycles were terminated earlierDraft in runs than riffles, as high expansion rates resulted in 37 patches reaching maximum mat size rapidly. Although M. autumnalis accrual differed among 38 rivers, this was attributed to differences in shear stress and grazing pressure rather than 39 nutrient concentrations. https://mc06.manuscriptcentral.com/cjfas-pubs Page 3 of 41 Canadian Journal of Fisheries and Aquatic Sciences 40 Introduction 41 Toxic planktonic cyanobacterial blooms have been a recognized water quality problem for 42 centuries (Francis 1878; Kirkby 1672; Paerl et al. 2001). Numerous studies investigating 43 physicochemical factors influencing the growth and bloom formation of planktonic species 44 have been undertaken, and a relatively robust understanding has developed (see(Oliver et al. 45 2012). In contrast, toxic benthic cyanobacterial proliferations have only recently become 46 recognized as an escalating problem in freshwater environments worldwide (Quiblier et al. 47 2013). Microcoleus autumnalis (formerly Phormidium autumnale) and closely related taxa 48 are benthic, mat-forming cyanobacteria which have become increasingly problematic in 49 cobble-bed rivers worldwide (Aboal et al. 2002; Fetscher et al. 2015; Gugger et al. 2005; 50 McAllister et al. 2016; Quiblier et al. 2013). M. autumnalis and closely related taxa produces 51 a variety of cyanotoxins including anatoxin-aDraft (ATX), homoanatoxin-a (HTX) and their 52 structural variants (Faassen et al. 2012; Fetscher et al. 2015; Gugger et al. 2005; Heath et al. 53 2010; Wood et al. 2007). Despite their ability to produce harmful toxins and the associated 54 health risk, the physicochemical factors causing proliferations in cobble-bed rivers are not yet 55 fully understood. 56 To date, most attempts to understand variables controlling the percentage of M. 57 autumnalis cover have examined reach-scale benthic mats dynamics and related these to 58 physicochemical factors measured in the surrounding environment (e.g.,(McAllister et al. 59 2018a; Wood et al. 2017). Such studies have implicated water chemistry, river flow and fine 60 sediment load as affecting M. autumnalis cover, though to date the predictive power of 61 statistical relationships generated is relatively weak (Heath et al. 2011; McAllister et al. 62 2018a; Wood et al. 2017; Wood et al. 2016). The difficulties in identifying key variables may 63 be complicated by the nature of the M. autumnalis accrual cycle. This involves colonisation, 64 initiation of a benthic mat, growth via patch expansion and eventual detachment. At each of https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 4 of 41 65 these successional phases, M. autumnalis is likely to respond differently to physicochemical 66 conditions (McAllister et al. 2016). 67 The spatial distribution of M. autumnalis mats in cobble-bed rivers is extremely 68 patchy, which has been partially attributed to small-scale differences in velocity (McAllister 69 et al. 2018a). The importance of velocity was reinforced by Hart et al. (2013) who noted that 70 in the field M. autumnalis was positively associated with velocity and generally dominated at 71 velocities >0.4 m s-1, and by Heath et al. (2015) who highlighted that cover was greatest 72 between 0.6 and 1.1 m s-1. The low-profile, dense, mucilaginous nature of M. autumnalis 73 mats, allows it to withstand higher velocities compared to other higher-profile species (Biggs 74 et al. 1998). High velocity environments are probably also conducive to M. autumnalis 75 accrual as the exchange of solutes at the mat-water interface is enhanced due to the reduction 76 of boundary layer thickness. McAllisterDraft et al. (2018b) showed that M. autumnalis biomass 77 accrual, but not mat expansion, was positively affected by an increase in velocity in 78 experimental mesocosms. However, the difference between velocity treatments was limited 79 (0.1 m s-1) and it is likely that larger differences in velocity would have elicited greater 80 responses in M. autumnalis accrual. 81 Field studies have also suggested that optimal ranges of nutrients may exist for M. 82 autumnalis accrual. Proliferations consistently occur at DRP concentrations below 0.02 mg L- 83 1 (McAllister et al. 2016; Wood et al. 2017; Wood et al. 2016). Optimal ranges for water- 84 column dissolved inorganic nitrogen (DIN) concentrations are less defined. Initially, 85 proliferations were thought to only occur when DIN was greater than 0.1 mg L-1 (Wood and 86 Young 2011; 2012), however, subsequent research has documented proliferations when DIN 87 concentrations are below 0.02 mg L-1 (McAllister et al. 2018a; Wood et al. 2017). Studies 88 investigating the effect of nitrate on M. autumnalis have included culture-based laboratory 89 investigations (Heath et al. 2016; Heath et al. 2014), observational field studies (Heath et al. https://mc06.manuscriptcentral.com/cjfas-pubs Page 5 of 41 Canadian Journal of Fisheries and Aquatic Sciences 90 2011; McAllister et al. 2018a; Wood et al. 2017) and most recently experimental mesocosms 91 (McAllister et al. 2018b). McAllister et al. (2018b) found that elevating nitrate concentrations 92 from 0.02 mg L-1 to 0.4 mg L-1 did not elicit a significant increase in M. autumnalis biomass 93 accrual (chlorophyll a concentrations and biovolumes) or patch expansion rates. 94 An important commonality among observational-based field studies on M. autumnalis 95 is that even after the inclusion of a wide range of physicochemical factors, “site” remains a 96 key determinant of reach-scale cover (McAllister et al. 2018a; Wood et al. 2017). This 97 suggests that time-independent, site-specific attributes are important in determining M. 98 autumnalis cover, but are missing from analyses to date. One factor, which remains largely 99 unexplored, despite its general importance in controlling periphyton growth, is herbivory 100 (Anderson et al. 1999; Karouna and Fuller 1992). The extent to which herbivorous 101 macroinvertebrate communities influenceDraft algal growth depends on factors including the 102 mobility, feeding rates, life-history timing, body size, and density of each species 103 (Holomuzki et al. 2010; Steinman 1996). Velocity also influences the removal of algae by 104 macroinvertebrates and can influence their density and composition (Hintz and Wellnitz 105 2013). 106 In the present study, variation in M. autumnalis biomass accrual and expansion was 107 investigated across gradients of velocity (pools, runs and riffles) in three rivers with varying 108 water chemistry. Cobbles were manually inoculated with M. autumnalis (McAllister et al. 109 2018b) which allowed the colonisation step of the accrual cycle to be standardized. The 110 following

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