Herbivore abundance, site fidelity and grazing rates on temperate reefs inside and outside marine reserves

Journal of Experimental Marine Biology and Ecology 478 (2016) 96–105

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Herbivore abundance, site fidelity and grazing rates on temperate reefs inside and outside marine reserves Adrian M. Ferguson a,b,⁎, Euan S. Harvey c, Nathan A. Knott d,b a

The UWA Oceans Institute and School of Plant Biology, The University of Western Australia, Crawley, WA 6009, Australia Institute for Conservation Biology and Environmental Management, School of Biological Sciences, University of Wollongong, NSW 2522, Australia Department of Environment and Agriculture, Curtin University, Bentley, WA 6102, Australia d NSW Department of Primary Industries, Jervis Bay Marine Park, 4 Woollamia Road, Huskisson, NSW 2540, Australia b c

a r t i c l e

i n f o

Article history: Received 27 May 2015 Received in revised form 20 February 2016 Accepted 22 February 2016 Available online xxxx Keywords: Acoustic telemetry Algae Fish Girellidae Herbivory Kyphosidae Marine protected area

a b s t r a c t A key objective of marine reserves is to maintain ecological processes important to the functioning of marine ecosystems. Grazing by tropical herbivores contributes to maintaining resilient coral reefs and marine reserves are critical in conserving herbivores and the functional role they provide. Less is known, however, about the effects of marine reserves on herbivorous fish and their role on temperate reefs. This study evaluated the potential for marine reserves to enhance grazing by herbivores on temperate reefs in Jervis Bay Marine Park, Australia. First, the movement patterns of a dominant grazer, luderick Girella tricuspidata, were determined using acoustic telemetry to assess the potential effects of marine reserves on G. tricuspidata. Second, the size and abundance of G. tricuspidata and other grazers (rock blackfish Girella elevata and silver drummer Kyphosus sydneyanus) was quantified on shallow subtidal reefs inside and outside marine reserves using a diver operated stereo-video system. Finally, grazing rates were quantified inside and outside marine reserves using video cameras. Luderick G. tricuspidata exhibited strong site fidelity on shallow subtidal reefs and was significantly larger and more abundant within marine reserves. Rock blackfish G. elevata was significantly more abundant in one of four marine reserves, although showed no difference in size between zones. Silver drummer K. sydneyanus was significantly larger in marine reserves, although not significantly more abundant. On shallow subtidal reefs, G. tricuspidata was the dominant grazer compared to other girellids and kyphosids, accounting for N97% of total algal bites (predominantly on algal turfs). Grazing rates were higher on average within marine reserves (although not significantly higher) and there was a positive correlation between the relative abundance of G. tricuspidata and number of algal bites, indicating grazing intensity increased with abundance. The findings in this study demonstrate the clear potential for greater grazing by herbivores within temperate marine reserves. This study also suggests that exploitation of targeted herbivores on temperate reefs is significant and marine reserves can reduce this impact and allow it to be measured via reference areas. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Marine reserves are used as a management tool to protect and conserve biodiversity and marine habitats against a range of human impacts including habitat degradation, climate change and overfishing (Ballantine, 2014). While generally not designed solely as a fisheries management tool, the establishment of marine reserves has resulted in significant increases in the size and abundance of targeted species (Roberts et al., 2001; Halpern, 2003; Lester et al., 2009; Edgar et al., 2014). These increases have led to complex changes to marine ecosystems within reserves as the strength of trophic interactions between species are affected, ⁎ Corresponding author at: The UWA Oceans Institute and School of Plant Biology, The University of Western Australia, Crawley, WA 6009, Australia. E-mail addresses: [email protected] (A.M. Ferguson), [email protected] (E.S. Harvey), [email protected] (N.A. Knott).

http://dx.doi.org/10.1016/j.jembe.2016.02.008 0022-0981/© 2016 Elsevier B.V. All rights reserved.

providing insight into the ecosystem-wide effects of overfishing (Babcock et al., 1999; Edgar and Barrett, 1999; Shears and Babcock, 2003; Edgar et al., 2009). As a result, more research has focussed on the role of marine reserves in maintaining ecological processes essential to ecosystem integrity (Olds et al., 2012) and this is now widely included as key objective of marine park legislation (e.g. South Australian Marine Parks Act, 2007, New South Wales Marine Estate Act, 2014). The establishment of marine reserves in both temperate and tropical systems has seen several striking examples of a reversal of the effects of overfishing on marine ecosystems. On coral reefs, herbivorous fish play a key ecological role grazing algae, which in turn promotes coral growth and recruitment and helps maintain reef resilience (Hughes et al., 2007). Declines in herbivore populations as a result of overfishing have contributed to phase shifts from coral-dominated reefs to degraded systems where macroalgae dominate (Hughes et al., 2003, 2010; Bellwood et al., 2004). Greater biomass of targeted herbivores and

A.M. Ferguson et al. / Journal of Experimental Marine Biology and Ecology 478 (2016) 96–105

increased grazing within marine reserves, however, has been shown to lower macroalgal cover, potentially preventing phase shifts from coralto algal-dominated systems (Mumby et al., 2006; Harborne et al., 2008; Rasher et al., 2013). On temperate reefs sea urchins are considered to be the major grazers (Jones and Andrew, 1990) and intense grazing by high densities of sea urchins (due to overharvesting of sea urchin predators i.e. lobsters and predatory fish) has resulted in phase shifts from kelp forests to urchin barrens (Estes et al., 1998; Sala et al., 1998; Babcock et al., 1999; Shears and Babcock, 2002). Shears and Babcock (2003) demonstrated, however, that benthic communities within a New Zealand marine reserve shifted from being dominated by sea urchins and barrens habitat to being dominated by kelp forests, which was attributed to the recovery of populations of lobsters and predatory fish within the reserve. Compared to coral reefs the ecological importance of fish herbivory on temperate reefs is more contentious. Few species are strictly herbivorous and fish herbivory is generally considered to have a minor impact on algal community structure (Jones and Andrew, 1990; Andrew, 1999), although an increasing number of studies are beginning to challenge this notion (Sala and Boudouresque, 1997, Ojeda and Munoz, 1999; Vergés et al., 2009; Taylor and Schiel, 2010; Bennett et al., 2015). For example, Bennett et al. (2015) showed that herbivores on temperate reefs had significant effects on algal communities and displayed feeding rates comparable to those on global coral reefs. Furthermore, the effects of herbivores on temperate reef algal communities are predicted to increase with the climate-driven range expansion of tropical herbivores onto temperate reefs as waters warm (Verges et al., 2014; Bennett et al., 2015). On temperate reefs in Australasia species from the closely related families Girellidae and Kyphosidae can form a significant component of the total fish biomass and have been shown to be important grazers (Russell, 1977; Jones, 1988; Kingsford, 2002; Bennett et al., 2015). In south-eastern Australia, the three commonly occurring species are luderick Girella tricuspidata (Quoy and Gaimard, 1824), rock blackfish Girella elevata (Macleay, 1881) and silver drummer Kyphosus sydneyanus (Günther, 1886) (Hutchins and Swainston, 1999). The zebra fish Girella zebra (Richardson, 1846) also occurs in southern Australia, although it is relatively uncommon in New South Wales (NSW) (Hutchins and Swainston, 1999). These species are primarily herbivorous, feeding mainly on macroalgae (Russell, 1983; Choat and Clements, 1992; Clements and Choat, 1997; Moran and Clements, 2002; Raubenheimer et al., 2005), and are most abundant in shallow water (Kingsford, 2002). They are also exploited by commercial and recreational fishers in Australia and girellids are amongst the most targeted recreational species caught on reefs in NSW (Lincoln Smith et al., 1989; Kingsford et al., 1991; Kingsford, 2002). For example, G. tricuspidata's current exploitation status in NSW is fully fished (WFRP, 2010a) and the combined commercial and recreational catch in NSW alone is between ~700 and 1000 t annually (Gray et al., 2012). Similarly, G. elevata is targeted by recreational fishers and there are concerns that stocks have been significantly depleted by overfishing, however, limited biological or fisheries data exist on which to base reliable assessments (WFRP, 2010b). Silver drummer K. sydneyanus is also targeted by fishers in NSW, although not as heavily as both G. tricuspidata and G. elevata (Kingsford, 2002). Girellids and kyphosids are therefore model species for which to assess the potential effects of fishing on their functional role as grazers on temperate reefs, due to their high level of exploitation. Furthermore, significant fishing effort (e.g. rock fishing, spearfishing and boat fishing) is concentrated in shallow subtidal areas (i.e. 1 to 3 m depth) where these species occur (Lincoln Smith et al., 1989; Kingsford et al., 1991; Smallwood et al., 2006) and any associated impacts would be predicted to be greatest, however, few studies have examined the effects of marine reserves in these areas (Coleman et al., 2013). Understanding movement patterns is also key to assessing the potential effects of marine reserves on targeted species (Welsh and Bellwood, 2014). Marine reserves can only be effective if they include a significant

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part of the home range of targeted species, during at least part of their life cycle (Kramer and Chapman, 1999). Often studies quantifying the size and abundance of targeted species inside and outside marine reserves are done without knowledge of movement patterns in relation to marine reserve design and vice versa. Luderick G. tricuspidata is considered to be highly mobile (Kingsford, 2002; Curley et al., 2013) and mark-recapture experiments carried out in NSW have shown that some tagged fish can move distances up to 450 km from their point of release (Thomson, 1959; Gray et al., 2012). It is for this reason that G. tricuspidata is considered unlikely to benefit from marine reserves (Kearney, 2007). Despite these relatively large movements, markrecapture experiments have shown that the majority of tagged G. tricuspidata recaptured were caught within the same estuary in which they were released (Thomson, 1959; West, 1993; Gray et al., 2012), in some instances nearly two years later, indicating residency within those estuaries. Initial acoustic tracking data has also demonstrated G. tricuspidata exhibit strong site fidelity on shallow subtidal reefs over a three month period (Ferguson et al., 2013). Preliminary data on the movements of G. elevata and K. sydneyanus also indicates both species display residency on reefs (Stocks et al., 2014; Pillans et al., 2011). Species that exhibit strong site fidelity would be predicted to benefit (through greater size and abundance) from marine reserves which include all or part of their home range if exploitation levels are significant.

Fig. 1. Map of Jervis Bay, New South Wales, Australia, where the study was conducted. Boxed areas (with the exception of BNP) represent marine reserves. Fish surveys were carried out at a total of 18 sites inside and outside marine reserves (marked with an X). Feeding observations were carried out at a subset of 8 sites (marked with an X). Shaded transparent areas represent Blocks 1–4 (numbered) determined a priori and used in the analyses. Rocky reef (gray) and seagrass (hatch) habitats are shown. An inset map of Australia indicating the study area is also shown.

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A.M. Ferguson et al. / Journal of Experimental Marine Biology and Ecology 478 (2016) 96–105

The main objective of this study was to assess the potential for marine reserves to enhance grazing by girellids and kyphosids on shallow subtidal reefs in Jervis Bay Marine Park, NSW, Australia. Specifically, this study assessed (i) movement patterns of G. tricuspidata in relation to marine reserves, using acoustic telemetry, (ii) the size and abundance of girellids and kyphosids on shallow subtidal reefs inside and outside marine reserves, and (iii) grazing rates of girellids and kyphosids on shallow subtidal reefs inside and outside marine reserves. It was predicted that (i) G. tricuspidata would exhibit strong site fidelity on shallow subtidal reefs and, therefore (ii) the size and abundance of G. tricuspidata, as well as G. elevata and K. sydneyanus (based on current information on the movement patterns of these species) would be greater within marine reserves, and (iii) grazing rates would be related to abundance, and hence higher within marine reserves. 2. Material and methods 2.1. Study area The study was carried out in Jervis Bay (35°08′S 150°43′E), a large embayment in southern NSW, Australia (Fig. 1). Jervis Bay forms the central area of Jervis Bay Marine Park (JBMP), which covers an area of approximately 21,100 ha. Jervis Bay Marine Park is a multiple-use marine park zoned for various activities within different management zones. Approximately 20% of JBMP is zoned as “no-take” sanctuary zones (hereafter referred to as marine reserves), 72% as habitat protection zones (HPZs) (recreational fishing, including collecting/harvesting, and some forms of commercial fishing allowed), 8% as general use zones and 0.2% as special purpose zones. Commonwealth waters of Booderee National Park (BNP) are also located within Jervis Bay, in which only recreational line fishing is allowed (spearfishing and collecting/harvesting are prohibited) (Fig. 1). The zoning plan for JBMP was implemented in 2002 and fishing restrictions had been in place for approximately nine years prior to the commencement of this study. Jervis Bay Marine Park represents an ideal system in which to test for differences between management zones because it contains multiple, spatially independent marine reserves and adjacent fished areas within which replicate habitat types occur i.e. intertidal and subtidal reefs and seagrass beds, interspersed with soft sediments.

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patterns found over time. To determine whether there was a difference in the size and abundance of girellids and kyphosids between protected and fished areas, two to three sites were surveyed within each of four marine reserves and four adjacent habitat protection zones or BNP waters respectively (Fig. 1). Total abundance was quantified at each site along six 50 × 5 m transects by a snorkeler using a diver operated stereo-video system (stereo-DOVS) (Harvey and Shortis, 1995). This technique enabled precise and accurate estimates of fish length (Harvey et al., 2002). Surveys were done in 1–3 m depth below mean sea level and transects ran parallel to the shoreline. A hip chain attached to the stereo-DOVS was used to measure the distance of each transect. Biodegradable cotton thread was attached to the reef at the start of each transect and unwound until the hip chain counter showed a distance of 50 m had been travelled. Transects were separated by a minimum distance of 20 m. To provide robust estimates of total abundance, each site was surveyed twice within each period during daylight hours (0900–1700 h) and the order in which sites were surveyed was determined randomly. 2.4. Image analysis Video imagery collected during the fish surveys was analysed using the software program EventMeasure (Stereo) (SeaGIS; www.SeaGIS. com.au). For each transect, all fish observed within the families Girellidae and Kyphosidae were identified to species level, counted and their length measured if possible. Measurement constraints were set within EventMeasure so that fish were only counted and measured if they came within a range of 5 m in front of the cameras and 2.5 m either side of the cameras to ensure a standardised sampling area. 2.5. Feeding observations

Long term movement patterns for G. tricuspidata were assessed as described in Ferguson et al. (2013). Six fish were surgically implanted with acoustic transmitters and passively tracked over an eleven month period from December 2011 to October 2012, using a fixed array of twenty receivers deployed on the majority of shallow subtidal reefs around the edge of Jervis Bay. Luderick G. tricuspidata was caught and released on shallow subtidal reefs within a marine reserve and BNP waters to assess movements within and between management zones. The movement data presented here represents data collected over the entire eleven month life of the acoustic transmitters (i.e. ~286 d), subsequent to the three months of data presented in Ferguson et al. (2013).

To determine whether grazing rates were higher inside marine reserves (and if there was a relationship between relative abundance and grazing rates) feeding observations were carried out at a representative subset of eight of the eighteen sites that fish surveys were carried out at, during March to April 2013 (Fig. 1). Observations were made at one site within each of four marine reserves and four adjacent habitat protection zones or BNP waters (Fig. 1). At each site, five replicate video cameras (GoPro HD Hero2; gopro.com) mounted on bricks were deployed on the reef in 1–3 m depth, within the same habitat sampled during the fish surveys (i.e. algal turfs interspersed with large brown macroalgae). Video cameras were separated by a minimum distance of 50 m. Grazing intensity was measured as the number of algal bites taken by all girellids and kyphosids within a 2 m2 area over a 2 h sampling period. The relative abundance or MaxN (i.e. the maximum number of individuals of any one species captured in a frame during the sampling period) of all girellids and kyphosids was also recorded for each replicate at each site. To provide more robust estimates of number of algal bites for each species, feeding observations were carried out twice at each site on separate days during daylight hours (0900–1700 h), giving a total of 20 h feeding observations per site. The order in which feeding observations were carried out at sites was determined randomly.

2.3. Fish surveys

2.6. Statistical analyses

Fish surveys were carried out at eighteen sites, comprising the majority of shallow subtidal reefs within Jervis Bay (Fig. 1). Surveys were carried out during two time periods; (i) February to March and (ii) October to November 2011, to assess the consistency of any spatial

To assess the level of site attachment G. tricuspidata exhibited on shallow subtidal reefs in JBMP a Residency Index (RI) was calculated as described in Ferguson et al. (2013). This was calculated as the total number of detection days for each fish on each receiver, divided by

2.2. Fish movements

Fig. 2. Site fidelity exhibited by Girella tricuspidata on shallow subtidal reefs in Jervis Bay, New South Wales, Australia, determined using acoustic telemetry. Fish 9–14 are shown in separate panels. Numbers identifying individual fish correspond with those presented in Ferguson et al. (2013). Abbreviated site names where individual fish were caught and released are shown in the respective panels (e.g. fish 9 was caught and released at GBN). Boxed areas (with the exception of BNP) represent marine reserves. Graduated symbols and adjacent values represent Residency Indexes (RI) (i.e. the total number of actual detection days for each fish on each receiver divided by the total number of possible detection days, multiplied by one hundred to express as a percentage). Empty circles represent receivers that received no detections.

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the total number of possible detection days and multiplied by one hundred to express as a percentage. To test whether there was a significant difference in the total abundance of G. tricuspidata, G. elevata and K. sydneyanus between marine reserves and fished areas, data for each species were analysed using a five-factor permutational multivariate analysis of variance (PERMANOVA) (Anderson, 2001a). Although univariate data sets, PERMANOVA was used instead of ANOVA because the permutational test requires no specific assumptions regarding number of variables or type of distribution (Anderson, 2001b). Factors included: Period (2 levels and random), Time (2 levels nested within Period and random), Status (2 levels and fixed: marine reserve and fished), Block (4 levels and random) and Site (2–3 levels nested within Block × Status and random). Marine reserves and adjacent fished areas were grouped into Blocks a priori based on proximity and environmental factors (e.g. orientation, exposure). Abundance analyses were done on fourth root transformed data using Euclidean distance measures. To test whether there was a significant difference in the size of G. tricuspidata between marine reserves and fished areas, data were analysed using the same PERMANOVA design described above. Mean size per transect was used for the analysis. The size analysis was done on untransformed data using Euclidean distance measures. Due to the patchy distribution of both G. elevata and K. sydneyanus the Kolmogorov–Smirnov 2 sample test (K–S test) was used instead to determine whether length distributions differed between marine reserves and fished areas for both species. To test whether there was a significant difference in grazing rates inside and outside marine reserves, data were analysed using a two-factor PERMANOVA. Factors included: Status (2 levels and fixed: marine reserve and fished) and Block (4 levels and random). The analysis was done on untransformed data using Euclidean distance measures. Simple linear regression was used to test for a relationship between mean grazing rates and mean relative abundance of girellids and kyphosids. Both response and predictor variables were log (natural) transformed to improve normality and homogeneity of variances. Replicate quadrats for each site were pooled across time to give a total of 10 replicate quadrats per site for the analysis.

3. Results 3.1. Fish movements Strong site fidelity was exhibited by G. tricuspidata on shallow subtidal reefs over the entire eleven month tracking period. For all six fish tracked, the Residency Index (RI) was highest at release reefs (Fig. 2). On average, fish were detected for 64% of days on release reefs and two fish (fish 12 and 14) were detected for ≥90% of days on release reefs. Fish did make regular movements between adjacent reefs over relatively small distances (i.e. hundreds of metres to kilometres), although consistently returned to release reefs. Only one fish (fish 13) was detected leaving the array, which occurred after approximately one and a half months of tracking, before being later detected in a neighbouring array in an estuary ~90 km south of Jervis Bay. Of the four fish released within the marine reserve, only one (fish 9) was detected moving outside the reserve over the entire tracking period (Fig. 2). This involved a single trip over a minimum distance of ~ 8 km, before returning to the reserve and its release reef. Of the two fish caught and released outside the marine reserve in BNP waters, one fish (fish 14) moved over an equivalent spatial scale to those fish tagged within the reserve and had the highest RI of all tagged fish, being detected on its release reef for 96% of days over the eleven month tracking period. The other fish (fish 13) was not detected within the array again during the eleven month tracking period, after leaving the array following approximately one and a half months of tracking.

3.2. Fish surveys On shallow subtidal reefs, G. tricuspidata (total no. fish recorded = 2688) was the most abundant girellid or kyphosid, being approximately three times as abundant as G. elevata (total no. fish recorded = 908) and five times more abundant than K. sydneyanus (total no. fish recorded = 560). One zebra fish, G. zebra, was the only other species of girellid or kyphosid recorded during the surveys. Luderick G. tricuspidata was significantly more abundant within marine reserves (8.79 ± 1.12 per transect; mean ± S.E.) compared to fished areas (4.71 ± 0.78 per transect; mean ± S.E.) (Table 1, Fig. 3). Rock blackfish G. elevata was significantly more abundant in one of four marine reserves (i.e. Block 3), although there was no significant difference between marine reserves (3.54 ± 0.69 per transect; mean ± S.E.) and fished areas (1.14 ± 0.23 per transect; mean ± S.E.) overall (Table 1, Fig. 3). There was no significant difference in the abundance of K. sydneyanus between marine reserves (2.25 ± 0.62 per transect; mean ± S.E.) and fished areas (0.65 ± 0.21 per transect; mean ± S.E.) (Table 1, Fig. 3). As well as being more abundant, G. tricuspidata was significantly larger within marine reserves (296 mm ± 3 mm; mean ± S.E.) compared to fished areas (285 mm ± 3 mm; mean ± S.E.) (Table 2, Fig. 4). There was no significant difference in the distribution of lengths between marine reserves (260 mm ± 6 mm; mean ± S.E.) and fished areas (258 mm ± 10 mm; mean ± S.E.) for G. elevata (K–S test; P N 0.05). There was a significant difference in the distribution of lengths between marine reserves and fished areas for K. sydneyanus (K–S test; P b 0.05). Silver drummer K. sydneyanus was larger within marine reserves (312 mm ± 10 mm, mean ± S.E.) compared to fished areas (220 mm ± 14 mm, mean ± S.E.) (Fig. 4). 3.3. Feeding observations Luderick G. tricuspidata was the dominant grazer observed on shallow subtidal reefs compared to other girellids and kyphosids, accounting for N97% of total algal bites. Grazing by all other species of girellid (G. elevata and G. zebra) and kyphosid (K. sydneyanus) was rare (b 3% of total algal bites combined) (Table 3). Grazing rates were higher on average inside marine reserves (14.72 ± 10.73 m2 h−1, mean ± S.E.) compared to fished areas (8.51 ± 5.81 m2 h−1, mean ± S.E.), although not significantly higher (Tables 3 and 4, Fig. 5). There was a positive correlation, however, between the relative abundance of G. tricuspidata and number of algal bites (R2 = 0.85, d.f. = 7, P = 0.001), indicating grazing

Table 1 PERMANOVA table of results. Girella tricuspidata, Girella elevata and Kyphosus sydneyanus abundance on shallow subtidal reefs inside and outside marine reserves in Jervis Bay, New South Wales, Australia. Bold terms indicate a significant marine reserve effect. Pe = Period, St = Status, Bl = Block, Ti = Time and Si = Site. Source

d.f.

Girella tricuspidata MS

Girella elevata

P (perm) MS

Pe 1 2.148 0.521 St 1 24.452 0.002 Bl 3 16.915 0.003 Ti(Pe) 2 1.208 0.061 Pe × St 1 0.05 0.446 Pe × Bl 3 1.487 0.133 St × Bl 3 0.498 0.692 Si(St × Bl) 10 1.359 0.449 Ti(Pe) × St 2 0.155 0.890 Ti(Pe) × Bl 6 0.264 0.976 Pe × St × Bl 3 1.084 0.500 Pe × Si(St × Bl) 10 1.250 0.558 Ti(Pe) × St × Bl 6 1.283 0.505 Ti(Pe) × Si(St × Bl) 20 1.400 0.000 Residual 341 0.459 Total 412

0.158 8.643 4.504 0.009 0.991 0.07 2.026 0.626 0.675 0.220 0.222 1.197 0.341 0.406 0.415

Kyphosus sydneyanus

P (perm) MS

P (perm)

0.074 0.190 0.000 0.956 0.326 0.968 0.019 0.843 0.220 0.759 0.945 0.020 0.548 0.478

0.067 0.163 0.263 0.502 0.411 0.798 0.337 0.026 0.384 0.357 0.993 0.382 0.006 0.297

1.415 6.065 1.744 0.261 0.550 0.125 1.385 1.217 1.403 0.341 0.09 0.332 1.218 0.288 0.253

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intensity increased with abundance. Of the total number of algal bites taken by G. tricuspidata, 98% were on algal turfs and 2% were on large brown macroalgae (i.e. Fucales). In this study algal turfs are defined as being composed of numerous species (Chlorophyta, Rhodophyta and Phaeophyta), b 10 cm tall with filamentous and foliose morphology occurring as a mosaic of relatively small (~ 4 m2) to large patches (~ 250 m2) within intertidal to shallow subtidal areas (Connell et al., 2014).

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Table 2 PERMANOVA table of results. Girella tricuspidata size on shallow subtidal reefs inside and outside marine reserves in Jervis Bay, New South Wales, Australia. Bold terms indicate a significant marine reserve effect. Pe = Period, St = Status, Bl = Block, Ti = Time and Si = Site. Source

d.f.

MS

P (perm)

Pe St Bl Ti(Pe) Pe × St Pe × Bl St × Bl Si(St × Bl) Ti(Pe) × St Ti(Pe) × Bl Pe × St × Bl Pe × Si(St × Bl) Ti(Pe) × St × Bl Ti(Pe) × Si(St × Bl) Residual Total

1 1 3 2 1 3 3 10 2 6 3 10 6 16 182 249

5527.2 50,125 10,517 1438.5 5090.2 2690.1 3561 7566.9 435.07 981.68 8453.2 3666.5 391.45 704.7 650.07

0.277 0.049 0.224 0.287 0.638 0.636 0.917 0.095 0.404 0.291 0.052 0.003 0.742 0.371

4. Discussion 4.1. Patterns of size and abundance in relation to marine reserves and fished areas

Fig. 3. Mean (± S.E.) abundances of girellids and kyphosids on shallow subtidal reefs inside and outside marine reserves in Jervis Bay, New South Wales, Australia. The locations of Blocks 1–4 displayed on the x-axis are shown in Fig. 1. Asterisk (*) indicates Blocks that significantly differed in abundance of Girella elevata inside and outside marine reserves, determined using pairwise tests.

This study found that G. tricuspidata was significantly larger and more abundant within marine reserves. These findings are consistent with those predicted and indicate that marine reserves are having an effect on this species. Luderick G. tricuspidata is targeted by commercial and recreational fishers, including spearfishers, and is currently classified as fully fished (Kingsford et al., 1991; WFRP, 2010a). Commercial fishing (i.e. beach hauling) for G. tricuspidata also takes place within Jervis Bay, although specific statistics on annual catch rates are unavailable. Both G. elevata and K. sydneyanus appeared to show patterns in size and abundance consistent with effects predicted from protection, however not as strong or consistent as those of G. tricuspidata. Rock blackfish G. elevata was significantly more abundant in one of four marine reserves, although overall there was no difference between reserves and fished areas, and K. sydneyanus was significantly larger within reserves, although not significantly more abundant. Differences in the patterns of size and abundance between reserves and fished areas for these species may reflect differences in relative fishing pressure. Of all three species, G. tricuspidata is the most heavily targeted and showed the strongest effects of protection (in terms of greater size and abundance within reserves), whereas, K. sydneyanus is the least targeted and showed no significant difference in abundance between reserves and fished areas. Continued monitoring will provide a greater understanding of the response of these species to protection over time. No “before” data exists on the size and abundance of G. tricuspidata, G. elevata and K. sydneyanus on shallow subtidal reefs prior to the establishment of marine reserves in JBMP. This study effectively represents baseline data for these species and is therefore unable to unequivocally determine whether the patterns found were due to effects of protection, rather than due to underlying natural variation between sites in marine reserves and fished areas. Before data is important for assessing changes between reserves and reference areas when (i) only one marine reserve is established or (ii) when reserves are chosen on the basis that they represent unique areas (i.e. highly diverse communities or endemic species, spawning aggregations) (Coleman et al., 2013; Kelaher et al., 2014). For JBMP this was not the case, given that the marine park contains multiple reserves which were surveyed in this study to provide a robust test of the hypotheses and marine reserves did not represent unique areas, but rather were representative of surrounding habitats. Furthermore, given that the factor Status was replicated with multiple sites, times and periods, and stereo-DOVS transects were carried out on shallow subtidal reefs of

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Fig. 4. Size frequencies of girellids and kyphosids on shallow subtidal reefs inside and outside marine reserves in Jervis Bay, New South Wales, Australia. Mean length (±S.E.) and the number of fish sampled (n) are shown in each panel.

similar structure, randomly selected within marine reserves and reference areas, the experimental design used in this study makes it improbable that site specific factors were driving differences in the size and abundance of these species between reserves and fished areas. 4.2. Movement patterns in relation to marine reserves The findings in this study show that G. tricuspidata exhibits strong site fidelity on shallow subtidal reefs over relatively long periods of time, with some fish residing on release reefs for N90% of days over the eleven month tracking period. These findings are consistent with the movement patterns of other temperate reef fishes and demonstrate the importance of marine reserves in protecting diverse assemblages of

fishes covering a range of functional roles (Barrett, 1995; Lowry and Suthers, 1998; Parsons et al., 2010; Bryars et al., 2012; Stocks et al., 2014; Harasti et al., 2015). Previously it has been shown that G. tricuspidata display predictable patterns in movement between discrete daytime and night-time core use areas, likely used for feeding and sheltering respectively, indicating residency on reefs (Ferguson et al., 2013). Recent research has shown that G. elevata also exhibit strong site fidelity on shallow subtidal reefs, making few trips to nearby or adjacent reefs and remaining on release reefs for long periods of time (Stocks et al., 2014). Similar to G. tricuspidata, G. elevata also utilise core use areas within relatively small home ranges and display diurnal movement patterns, indicating residency on reefs (Stocks et al., 2014). Silver drummer K. sydneyanus has been shown to display limited

A.M. Ferguson et al. / Journal of Experimental Marine Biology and Ecology 478 (2016) 96–105

103

Table 3 Total number of algal bites taken by girellids & kyphosids on shallow subtidal reefs inside and outside marine reserves during feeding observations in Jervis Bay, New South Wales, Australia. Species

Total no. Relative proportion Total no. algal bites algal bites of total no. algal bites Marine reserve Fished

Girella tricuspidata 6698 Girella elevata 155 Kyphosus sydneyanus 5 Girella zebra 2 Total 6860

97.64% 2.26% 0.07% 0.03% 100%

4225 108 5 2 4340

2473 47 0 0 2520

movement on reefs centred around release locations, however, estimates of habitat use indicate K. sydneyanus have much larger home ranges than G. tricuspidata and G. elevata (Pillans et al., 2011). The strong site fidelity displayed by G. tricuspidata and G. elevata is consistent with the finding of greater abundance of both species within marine reserves (although G. elevata was significantly more abundant in only one of four reserves). Marine reserves can benefit targeted species where individuals or populations move mainly within localised home ranges encompassed by reserves, during at least part of their life cycle (Kramer and Chapman, 1999). This enhancement occurs because reserves provide relief from fishing pressure, which leads to an increase in local size, abundance and reproductive capacity (Russ et al., 2008; Bond et al., 2012). Silver drummer K. sydneyanus has been shown to display residency on reefs, although it occupies significantly larger home ranges than G. tricuspidata and G. elevata, which also exceeds the size of many reserves within JBMP (Pillans et al., 2011). This may be in part the reason why no significant difference was found in the abundance of K. sydneyanus inside and outside marine reserves, as K. sydneyanus moves over relatively larger areas and is more exposed to fishing pressure outside of reserves. The current knowledge on the movement patterns of G. tricuspidata and G. elevata highlights two important points in relation to the effects of marine reserves on both these species. First, both G. tricuspidata and G. elevata are relatively long-lived (N25 and N45 years respectively) (Gray et al., 2012; Stocks et al., 2014). Long-term site fidelity, therefore, should lead to significant increases in the size and abundance of both species within marine reserves over time, given the rate of fishing mortality is greater than that of natural mortality. Second, the strong site fidelity displayed by G. tricuspidata and G. elevata and utilisation of coreuse areas indicates both species consistently graze similar areas of reef which should lead to measurable effects on shallow water algal assemblages between marine reserves and fished areas over time. 4.3. Potential for enhanced grazing within marine reserves The findings in this study show that G. tricuspidata was the dominant grazer on shallow subtidal reefs compared to other girellids and kyphosids, accounting for N97% of algal bites, mostly on algal turfs. Given (i) the strong site fidelity displayed by G. tricuspidata, (ii) greater abundance and larger size of G. tricuspidata within marine reserves, (iii) higher average grazing rate inside reserves and (iv) positive correlation between G. tricuspidata abundance and number of algal bites, Table 4 PERMANOVA table of results. Number of algal bites by girellids and kyphosids on shallow subtidal reefs inside and outside marine reserves in Jervis Bay, New South Wales, Australia. St = Status and Bl = Block. Source

d.f.

MS

P (perm)

St Bl St × Bl Residual Total

1 3 3 69 76

47,309 3.0205E5 48,969 70,263

0.376 0.005 0.579

Fig. 5. Mean (±S.E.) number of algal bites by girellids and kyphosids on shallow subtidal reefs inside and outside marine reserves in Jervis Bay, New South Wales, Australia. The locations of Blocks 1–4 displayed on the x-axis are shown in Fig. 1.

these findings indicate shallow subtidal reefs within marine reserves in JBMP are receiving greater levels of grazing compared to fished areas. On average, grazing rates were higher inside marine reserves, although not significantly higher. This was due to a lack of statistical power to detect any difference in grazing rates inside and outside marine reserves. There was large variation in the number of algal bites recorded within and between sites in treatment and reference areas and greater replication was required to better estimate grazing rates inside and outside marine reserves. The main purposes of this section of the study, however, was to assess the relationship between the relative abundance of herbivores and grazing rates and relate this back to patterns of abundance found during the fish surveys, which provided a more reliable estimate of abundance inside and outside marine reserves. Substantially less grazing by G. elevata and K. sydneyanus was observed on shallow subtidal reefs compared to G. tricuspidata. Two possible explanations for this pattern are (i) both species were significantly less abundant than G. tricuspidata, therefore rarely observed during feeding observations, and (ii) G. elevata and K. sydneyanus were feeding in different habitats or at greater depths than G. tricuspidata. Nevertheless, G. elevata and K. sydneyanus most likely contribute to the level of grazing provided by G. tricuspidata on shallow subtidal reefs within reserves, given that both species appear to be responding positively to protection and also display some degree of site fidelity, including utilising core-use areas for feeding (Pillans et al., 2011; Stocks et al., 2014). This study provides estimates of grazing rates for girellids and kyphosids on temperate reefs inside and outside marine reserves. The effects of harvesting these herbivores on algal communities inside and outside reserves, however, need to be assessed. Greater grazing by G. tricuspidata within marine reserves may have important community-wide effects by altering the structure of shallow water algal assemblages. Luderick G. tricuspidata feed selectively on certain types of green and red algae (Choat and Clements, 1992; Clements and Choat, 1997; Curley et al., 2013) and may initially select reefs to reside on with higher cover of preferred algae (i.e. Ulva spp.) (Ferguson et al., 2015). Higher abundance combined with selective grazing by G. tricuspidata within marine reserves may therefore lead to differences in shallow water algal assemblages between reserves and fished areas. Ojeda and Munoz (1999) demonstrated that selective feeding by the herbivorous fish, Scartichthys viridis, on green (Ulva spp.) and red algae was important in determining algal community structure on temperate shallow subtidal reefs. Experimental exclusion of S. viridis resulted in increased abundance of Ulva spp., red foliose macroalgae and

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brown macroalgae, as well as an extension of the range of red macroalgae from the high to mid intertidal range. Based on the findings in this study, greater size and abundance of grazers on shallow subtidal reefs within marine reserves in JBMP should potentially lead to measurable differences between reserves and fished areas, in terms of algal community structure, over time. Future studies should be carried out to test and quantify this prediction. 4.4. Conclusion The findings in this study demonstrate the clear potential for greater grazing by herbivores within temperate marine reserves. This is significant, as it highlights the role marine reserves can play in maintaining this important ecological process on temperate reefs. Future assessment will provide insight into the effects of greater grazing within marine reserves on temperate reef communities. This study also suggests that human impacts, such as fishing, may have considerable effects on herbivores and the functional role they provide on temperate reefs and marine reserves can both reduce this impact and allow it to be measured via reference areas. Acknowledgements We thank all the staff at JBMP, in particular Matt Carr, Mark Fackerell and Ian Osterloh, as well as Luke van der Rijt and Bryce Dorrian for support with this study. We thank Karen Astles and four anonymous reviewers for constructive comments on the manuscript. We also acknowledge the assistance provided by the Australian Animal Tracking and Monitoring System (AATAMS). This research was approved by the Animal Ethics Committee of the Department of Environment, Climate Change and Water (NSW) (AEC Number: 100802/04), The University of Western Australia (RA/3/600/004) and (RA/3/100/1128) and the NSW Department of Primary Industries [scientific collection permits P09/0053-1.0 and P01/0059(A)-2.0]. [RH] References Anderson, M.J., 2001a. Permutation tests for univariate or multivariate analysis of variance and regression. Can. J. Fish. Aquat. Sci. 58, 626–639. Anderson, M.J., 2001b. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26, 32–46. Andrew, N., 1999. Under Southern Seas: The Ecology of Australia's Rocky Reefs. UNSW Press Ltd., Sydney, Australia. Babcock, R.C., Kelly, S., Shears, N.T., Walker, J.W., Willis, T.J., 1999. Changes in community structure in temperate marine reserves. Mar. Ecol. Prog. Ser. 189, 125–134. Ballantine, B., 2014. Fifty years on: Lessons from marine reserves in New Zealand and principles for a worldwide network. Biol. Conserv. 176, 297–307. Barrett, N., 1995. Short- and long-term movement patterns of six temperate reef fishes (families Labridae and Monacanthidae). Mar. Freshw. Res. 46, 853–860. Bellwood, D.R., Hughes, T.P., Folke, C., Nyström, M., 2004. Confronting the coral reef crisis. Nature 429, 827–833. Bennett, S., Wernberg, T., Harvey, E.S., Santana-Garcon, J., Saunders, B.J., 2015. Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs. Ecol. Lett. http://dx.doi.org/10.1111/ele.12450. Bond, M.E., Babcock, E.A., Pikitch, E.K., Abercrombie, D.L., Lamb, N.F., Chapman, D.D., 2012. Reef sharks exhibit site fidelity and higher relative abundance in marine reserves on the Mesoamerican Barrier Reef. PLoS One 7 (3), e32983. http://dx.doi.org/10.1371/ journal.pone.0032983. Bryars, S., Rogers, P., Huveneers, C., Payne, N., McDonald, B., 2012. Small home range in southern Australia's largest resident reef fish, the western blue groper (Achoerodus gouldii): implications for adequacy of no-take marine protected areas. Mar. Freshw. Res. 63, 552–563. Choat, J.H., Clements, K.D., 1992. Diet in odacid and aplodactylid fishes from Australia and New Zealand. Aust. J. Mar. Freshwat. Res. 43, 1451–1459. Clements, K.D., Choat, J.H., 1997. Comparison of herbivory in the closely-related marine fish genera Girella and Kyphosus. Mar. Biol. 127, 579–586. Coleman, M.A., Palmer-Brodie, A., Kelaher, B.P., 2013. Conservation benefits of a network of marine reserves and partially protected areas. Biol. Conserv. 167, 257–264. Connell, S.D., Foster, M.S., Airoldi, L., 2014. What are algal turfs? Towards a better description of turfs. Mar. Ecol. Prog. Ser. 495, 299–307. Curley, B.G., Jordan, A.R., Figueira, W.F., Valenzuela, V.C., 2013. A review of the biology and ecology of key fishes targeted by coastal fisheries in south-east Australia: identifying critical knowledge gaps required to improve spatial management. Rev. Fish Biol. Fish. 23, 1–24.

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