View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Nottingham ePrints Coral Reefs DOI 10.1007/s00338-017-1553-1 ORIGINAL PAPER Temperate macroalgae impacts tropical fish recruitment at forefronts of range expansion 1 1 2 1 H. J. Beck • D. A. Feary • Y. Nakamura • D. J. Booth Received: 15 October 2015 / Accepted: 25 January 2017 Ó Springer-Verlag Berlin Heidelberg 2017 Abstract Warming waters and changing ocean currents macroalgal habitat over temperate macroalgae for settle- are increasing the supply of tropical fish larvae to tem- ment in an aquarium experiment. This study highlights that perature regions where they are exposed to novel habitats, temperate macroalgae may partly account for spatial vari- namely temperate macroalgae and barren reefs. Here, we ation in recruitment success of many tropical fishes into use underwater surveys on the temperate reefs of south- higher latitudes. Hence, habitat composition of temperate eastern (SE) Australia and western Japan (*33.5°N and S, reefs may need to be considered to accurately predict the respectively) to investigate how temperate macroalgal and geographic responses of many tropical fishes to climate non-macroalgal habitats influence recruitment success of a change. range of tropical fishes. We show that temperate macroalgae strongly affected recruitment of many tropical Keywords Climate change Á Kelp forest Á Novel habitat Á fish species in both regions and across three recruitment Poleward range shift Á Temperate rocky reef Á Reef fishes seasons in SE Australia. Densities and richness of recruit- ing tropical fishes, primarily planktivores and herbivores, were over seven times greater in non-macroalgal than Introduction macroalgal reef habitat. Species and trophic diversity (K- dominance) were also greater in non-macroalgal habitat. Ocean warming is leading to rapid and widespread pole- Temperate macroalgal cover was a stronger predictor of ward shifts in the geographic distribution of many marine tropical fish assemblages than temperate fish assemblages, species (Thomas et al. 2004; Harley et al. 2006). This reef rugosities or wave exposure. Tropical fish richness, climate-driven redistribution of marine organisms is alter- diversity and density were greater on barren reef than on ing the composition and food web structure of coastal reef dominated by turfing algae. One common species, the ecosystems. Such climate-driven ecological changes often neon damselfish (Pomacentrus coelestis), chose non- negatively affect human societies that depend on coastal ecosystems for resources and economic stability (Cheung et al. 2009; Pereira et al. 2010). To manage ecological Communicated by Biology Editor Dr. Andrew Hoey impacts of climate change and their associated socioeco- nomic consequences (Burrows et al. 2014), accurate pre- Electronic supplementary material The online version of this dictions of the timing and location of species redistribution article (doi:10.1007/s00338-017-1553-1) contains supplementary material, which is available to authorized users. are required (Frusher et al. 2014). Nevertheless, factors that regulate the colonisation of new ranges are largely unre- & H. J. Beck solved (Hellmann et al. 2012; HilleRisLambers et al. 2013; [email protected] Urban et al. 2013). Certainly, supply of larval propagules 1 School of Life Sciences, University of Technology Sydney, into new ranges (Gaylord and Gaines 2000; Keith et al. Broadway, P.O. Box 123, Ultimo, NSW 2007, Australia 2011) and climate at higher latitudes (Pinsky et al. 2013) 2 Graduate School of Kuroshio Science, Kochi University, 200 may primarily determine how species respond to shifting Monobe, Nankoku, Kochi 783-8502, Japan isotherms. However, for reef-associated organisms, 123 Coral Reefs availability of suitable reef habitats may ultimately deter- common temperate brown algae, such as Ecklonia spp. mine whether they colonise higher latitudes (e.g. Hill et al. and Phyllospora spp., differ to that of tropical macroalgal 2001; Warren et al. 2001; Honnay et al. 2002; Travis 2003; communities, which are often dominated by Sargassum Cheung et al. 2010; Mair et al. 2014). spp. Temperate macroalgae also support different suites Changes in the extent and strength of poleward-flowing of biological communities (including potential predators currents may increase the thermal suitability of many and competitors) than tropical macroalgae (Kuiter 1993), temperate regions for tropical fishes (including Australia, which may influence tropical fish recruitment. Under- Japan, Korea, western Africa, Brazil and USA; Wu et al. standing at the seascape level how temperate macroalgae 2012;Beck2014). Temperate rocky reefs present a myriad influence recruitment of tropical fishes may allow man- of foreign biophysical conditions that may influence the agers to more accurately predict impacts of these invading poleward redistribution of tropical reef fishes. These novel species. These impacts so far include overgrazing of algae reef environments may determine where these fish recruit and increased competition for resources and predation (i.e. from settlement to reef habitat to survival to inclusion pressure on temperate reefs (Masuda et al. 2000;Feary in existing assemblages), and thus ultimately colonise, by et al. 2014;Verge´setal.2014). determining access to suitable resources. Interactions with Here, temperate coastal reefs of south-eastern (SE) native predators and competitors may also inhibit tropical Australia and western (W) Japan were used to investigate fish recruitment. However, the role of temperate reef how temperate macroalgal communities structure the habitats in influencing tropical fish recruitment currently density, richness and diversity of colonising tropical reef remains poorly understood (Beck 2014). To date, it has fishes. Many tropical fishes are supplied to SE Australia been shown that wave-protected temperate reefs offer a and W Japan by poleward-flowing boundary currents: the safe haven for many tropical fish recruits, at least at spatial East Australian Current in Australia and the Kuroshio scales of hundreds of metres (Beck et al. 2016a). Lower Current in Japan (Fig. 1). In these regions, tropical fishes densities of temperate predators are also known to improve commonly recruit to coastal temperate reefs throughout chances of overwinter success (Beck et al. 2016b). Warmer summer. Although cool waters currently constrain many winter water temperatures assist survival of tropical fishes of these warm-adapted fishes from surviving through by facilitating better physiological performance, hence winter, coastal waters in W Japan and SE Australia are improving access to resources, including food (Beck et al. warming at more than twice the global average (Wu et al. 2016b). 2012). Such rapid warming is expected to facilitate the A key remaining question is how temperate macroalgae ongoing colonisation of an increasing range of tropical impact tropical reef fish recruitment. Spatial heterogene- fish species (Figueira et al. 2009; Figueira and Booth ity in the physical structure, resources and associated 2010). temperate reef fish communities between temperate We examined the influence of temperate macroalgal macroalgal forests (canopy, subcanopy and basal layers) cover on recruitment of tropical reef fishes by comparing and patches of algal turf and/or barren reef (covered by the density, richness and diversity of new recruit and ephemeral or encrusting algae or bare reef; Curley et al. juvenile tropical fishes (hereafter termed ‘vagrants’) 2002) may lead to patchiness in tropical reef fish between macroalgal habitat (genera Ecklonia, Phyllospora recruitment (Shulman 1984, 1985; Beukers and Jones and Sargassum) and non-macroalgal habitats. Non- 1998;Almany2004). On coral reefs, many tropical reef macroalgal habitats were defined as consisting of low-lying fishes avoid algae-dominated areas. Such avoidance has turfing algae (Class Rhodophyta and Phylum Phaeo- previously been attributed to physical movement of algal phyceae) or barren rocky reef (rock covered in encrusting habitats in association with wave action, low availability and ephemeral Rhodophyta and Phaeophyceae, or bare of suitable fine-scale microshelter, higher predation risk rock with no algae). To examine factors that possibly in dense macroalgal areas and/or undesirable chemical contributed to differences in recruitment of tropical fishes cues from seaweed-dominated reefs (Hoey and Bellwood among non-macroalgal and macroalgal reef patches, reef 2011;Lecchinietal.2013;Dixsonetal.2014). Con- structure (topographical complexity), wave exposure, versely, a small proportion of tropical fish recruits have temperate reef fish community (including likely competi- been found to positively associate with the structural tors and predators) and benthic composition were also complexity and potential food sources provided by quantified. We conducted aquarium experiments using a macroalgal patches in tropical regions (Lecchini et al. common tropical damselfish (Pomacentrus coelestis) to test 2007; Wilson et al. 2010; Evans et al. 2014; Yamada et al. whether the observed habitat associations of vagrants 2012;Hoeyetal.2013). Tropical fishes may also respond resulted from preference during larval settlement (shift to macroalgae differently on temperate than tropical reefs. from pelagic to benthic life stage), rather than immigration For instance, the shape and movement characteristics of and/or differential mortality. 123 Coral Reefs Fig. 1 Survey sites (open circles)