Journal of the Royal Society of Western Australia, 103: 29–37, 2020 New perspectives on Western Australian seagrass and macroalgal biogeography DIANA WALKER 1 *, JOHN M HUISMAN 2, KIERYN KILMINSTER 1,3 & JOHN KUO 4 1 School of Biological Sciences, University of Western Australia, 35 Stirling Highway, Perth, WA 6009, Australia 2 Western Australian Herbarium, Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, 17 Dick Perry Avenue Kensington, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia 3 Department of Water and Environmental Regulation, WA Government, Locked Bag 10 Joondalup DC, WA 6919, Australia 4 Research Infrastructure Centres, University of Western Australia, 35 Stirling Highway, Perth, WA 6009, Australia * Corresponding author: [email protected] Abstract The widespread adoption of new methodologies, especially molecular techniques, has dramatically changed our understanding of how species of seagrasses and macroalgae are classified and distributed. One consequence of this new paradigm is increased uncertainty regarding biogeographic studies based on pre-molecular species records. The question “how does one delineate an individual species?” has changed and differing interpretations may alter how previous assessments are viewed. In some instances, specimens previously regarded as a single species have been shown to represent multiple genetic lineages. An extreme example is that of the red alga Portiera hornemannii, now thought to include 21 cryptic species in the Philippines alone, and possibly up to 96 species in the wider Indo-Pacific. Reworking and reclassification of species based on DNA analyses have sunk many species into one, or combined or reorganized genera. These changes in taxonomic concepts have implications for conservation and biogeographical assessments, but our understanding of many groups is still in its infancy and requires further work. In order to address these mounting challenges, significant investment and a commitment to taxonomic research will be required in the coming decades. Keywords: seagrass, macroalgae, taxonomy, biogeography, molecular sequencing Manuscript received 18 March 2019; accepted 4 March 2020 INTRODUCTION SEAGRASSES Seagrasses and macroalgae are important marine primary Western Australian waters are rich in seagrass species, producers that provide significant structural habitat both in diversity and areal extent. The history of seagrass in coastal waters (Walker & Bellgrove 2017; Bellgrove collectors and collections are summarised in Figure 1. The et al. 2018), and support diverse faunal communities state’s 26 currently recognized seagrass species represent (van der Heide et al. 2012). Western Australia is well- almost 40% of the world’s approximately 70+ known known as a centre of biodiversity for seaweeds and species (Kilminster et al. 2018; Larkum et al. 2018; Waycott seagrasses, with numerous species recorded and a et al. 2014), a concentrated diversity not found in any particularly high percentage of endemic taxa. Several other region. Western Australian seagrasses are widely recent publications have included detailed descriptions distributed across coastal areas and estuaries (Carruthers of the state’s marine flora (seagrasses in Larkum et al. et al. 2007) and a variety of habitats, although they are 2018; macroalgae in Huisman 2015, 2018) and this paper most commonly found associated with shallow, sandy does not reiterate those works. Rather, we will describe substrata. Most of the Western Australia’s temperate the history of marine plant biodiversity knowledge in species are endemic, while those occurring in tropical Western Australia, then discuss how new methodologies, waters are more widely distributed across the Indo- especially molecular techniques, have made dramatic Pacific region. A list of currently recognised species across changes to our understanding of how species of all of the Western Australian coast (Table 1) is divided seagrasses and macroalgae are classified and distributed. into three major regions (South West, South-Coast, and The implications of these changes may be significant, Tropical WA) with dominant species life history strategies with real impacts on marine biodiversity assessments, (colonising, opportunistic or persistent, sensu Kilminster and potential impacts on environmental legislation. et al. 2015) also indicated. The published patterns of distribution and biogeography have changed little from the earlier historical records summarised in Walker (1991). The historical and present-day drivers shaping biogeography © Royal Society of Western Australia 2020 patterns are explored and distributional changes due to 29 Journal of the Royal Society of Western Australia, 103, 2020 Ferninand von Mueller4 appointed as government botanist of Victoria in 1853 Robert Brown1 visited aboard HMS Investigator Jacques Labillardière2 (1807) Phytographiae Australiae (1872–74) (1801–03) described Ruppia antarctica lists 9 Australian seagrasses (now Amphibolis antarctica) Paul Ascherson5-7, likely sent Zostera muelleri, Z. tasmanica, Collected and described specimens from explorers J D Hooker3 (1858) described Cymodocea serrulata, C. ciliata (now termed ‘Seegräser’ in 1871 four Australian seagrasses Posidonia australis Thalassodendron ciliatum), C. antarctica (now under the generic name Amphibolis antarctica), Posidonia australis, Described eight genera, Caulinia Halophila ovata (now Halophila ovalis), Caulinia spinulosa (now Halophila spinulosa) six tribes, two families and Enhalus koenigii (now Enhalus acoroides) (~20 species world-wide) Ducker et al.12 reviewed the The Sea-grasses of the World Amphibolis genus in 1977 Carl Ostenfeld9 described a published by den Hartog11 in1970 new species Cymodocea 10 13,14 8 Doty & Stone Kuo & Cambridge J M Black described angustata (1914). Pectinella grithii as described Halophila Recognised 49 species, redened Posidonia genus Did not support Amphibolis australis (1966) 12 genera, with three species in the P. a new species (1915). antarctica and A. grithii as 6 sub-families and australis group (1979) and ve Introduced generic separate species (1916). name of Pectinella for 2 families world-wide species in the P. ostenfeldii group (1984) the species now In 1929, listed 15 known as Amphibolis Listed 23 species as occuring Australian seagrasses In 1980s, genetic approaches to antarctica and in seven genera and in Australia including 3 new species A. grithii but in his Zostera mucronata, study Australian seagrasses began two families 15-18 ora treatment Thalassodendron pachyrhizum (McMillan and coworkers ) (1922–24) reverted and Posidonia ostenfeldii and since then both molecular to generic name of and taxonomic evidence used for Cymodocea species classication (e.g. Jacobs & Les19,20) 1 Brown R (1960) 8 Black J M (1915, 1922–24) 15 McMillian C (1982), (1983a, 1913b, 1986, 1991) 2 Labillardière J J H (1807) 9 Ostenfeld C H (1914, 1916, 1929) 16 McMillian C and Williams S C (1980) 3 Hooker J D (1858) 10 Doty M S and Stone B C (1966) 17 McMillian C, Williams SC, Escobar I,and Zapata O (1981) 4 Mueller F von (1872–74, 1886, 1902) 11 den Hartog (1970) 18 McMillian C, Young P C, Cambridge M C, Masini R and 5 Ascherson P (1868, 1871, 1875, 1906) 12 Ducker S C, Foord N J and Knox R B (1977) Walker D I (1983) 6 Ascherson P and Graebner P (1907) 13 Cambridge M L and Kuo J (1979) 19 Les D H, Moody M L, Jacobs, S W L and Bayer R J (2002) 7 Ascherson P and Gürke M (1889) 14 Kuo J and Cambridge M L (1984) 20 Jacobs S W L and Les D (2009) Figure 1. A selection of notable botanists and their contributions to Australian seagrass knowledge from 1800–2010. anthropogenic and climate impacts for the south-west of seagrass in Shark Bay as a response to the 2011 marine Western Australia are reported in Kilminster et al. (2018). heatwave (Ariaz-Ortiz et al. 2018; Kilminster et al. 2018). It is likely that climate-driven changes will alter the Recent seagrass research in Western Australia has biogeography of seagrasses in the region in decades to primarily focused on ecophysiological aspects or studies come. of recruitment and population structure. Many of the ecophysiological studies have shifted in focus to the Over the last decade, 10 new species have been added roots and rhizomes of seagrasses, specifically exploring to the Australian seagrass flora (Larkum et al. 2018), relationships between sediment biogeochemistry, but several of these are reclassifications of existing seagrass health and the microbes that inhabit the records and their validity is the subject of much debate seagrass rhizosphere (Fraser et al. 2017; Kilminster et al. (Waycott et al. 2018). Kuo (2005) found that Heterozostera 2014; Martin et al. 2019; Martin et al. 2018; Olsen et al. was not a monotypic genus but consisted of at least 2018). A conservation and restoration agenda has driven three Australian species. He redefined H. tasmanica and the studies of recruitment and population structure, described two new species, H. nigricaulis J. Kuo and H. with enhanced understanding of the potential of seed- polychlamys J. Kuo, in the process removing H. tasmanica based restoration, recruitment-bottlenecks and genetic from the Western Australia flora. Jacobs & Les (2009) connectivity between populations (Kendrick et al. 2017; formally rejected Heterozostera as a genus and transferred McMahon et al. 2017; McMahon et al. 2018; Sinclair et al. the two new described Heterozostera species into the 2018; Statton et al. 2017a;