1 Testing ocean warming solutions for red abalone Haliotis rufescens mariculture in San 2 Jeronimo Island, , Mexico: Effects of depth and diet 3 4 5 Jeremie Bauer1, Rodrigo Beas-Luna1, Julio Lorda*2, Luis Malpica-Cruz3,4, Fabiola Lafarga 6 -De la Cruz5; Fiorenza Micheli6, Ricardo Searcy-Bernal7, Laura Rogers-Bennett8, Miguel 7 Bracamontes-Peralta9.

8 9 1Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, Carretera 10 Ensenada- 3917, Fraccionamiento Playitas, 22860 Ensenada, Baja California, 11 México

12 2Facultad de Ciencias, Universidad Autónoma de Baja California, Carretera Ensenada- 13 Tijuana 3917, Fraccionamiento Playitas, 22860 Ensenada, Baja California, México.

14 3Instituto de Investigaciones Oceanológicas, Universidad Autónoma de Baja California, 15 Carretera Ensenada-Tijuana 3917, Fraccionamiento Playitas, 22860 Ensenada, Baja 16 California, México.

17 4ECOCIMATI, A.C., Av. del Puerto 2270 Colonia , 22880 Ensenada, Baja 18 California, Mexico.

19 5Departamento de Acuicultura, Centro de Investigación Científica y de Educación 20 Superación de Ensenada, Carretera Ensenada-Tijuana No. 3918, Zona Playitas, CP 22860, 21 Ensenada, Baja California, Mexico.

22 6Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950, USA

23 7Instituto de Investigaciones Oceanológicas, Universidad Autónoma de Baja California, 24 Carretera Ensenada-Tijuana 3917, Fraccionamiento Playitas, 22860 Ensenada, Baja 25 California, México (Retired).

26 8California Department of Fish and Wildlife and Bodega Marine Laboratory, University of 27 California, Davis, PO Box 247, Bodega Bay, CA 94923, USA 28 9Sociedad Cooperativa de producción Pesquera “Ensenada”. El Rosario, Baja California, 29 Mexico.

30 *Corresponding author. Email: [email protected]

31 Abstract

32 Wild abalone fishery landings have decreased significantly in past decades as global 33 abalone aquaculture has increased drastically shifting production from fishing to farming. 34 In California (USA) and Baja California (Mexico), multiple climatic stressors and 35 overfishing are thought to be responsible for mass mortalities and the significant decline of 36 abalone resources. One alternative for supporting sustainable abalone fishing is captive 37 propagation and subsequent restocking into the wild. To test, inform, and promote 38 innovative sustainable seafood production strategies in the Northeastern Pacific, we 39 designed an experimental mariculture system at San Jeronimo Island, Baja California in 40 collaboration with the local fishing cooperative. Specifically, the aim was to explore the 41 feasibility of rearing red abalone seed, Haliotis rufescens, on a mariculture setting, to 42 achieve a larger size for future local restocking programs. We tested the effects of two 43 different depths for growing abalone, surface and bottom (5 m) and three different 44 macroalgae diets (Macrocystis pyrifera, Ecklonia arborea and a mixed diet of M. 45 pyrifera/Pelagophycus porra) on the survival and growth of juvenile red abalone (32 ± 3.33 46 mm), inside cages attached to a long line system. The experiment lasted 90 days and the 47 red abalone, mean daily increment in shell length was 87 ± 13 µm d-1. The total mean 48 growth in shell length was 7.86 ± 1.13 mm or 2.62 ± 0.38 mm m-1, with 97% survival 49 rate. Depth did not affect abalone growth or survival. There were no significant differences 50 in growth among abalone fed with the three diets; however, E. arborea fed abalone grew 51 more than those fed with M. pyrifera and the mixed diet. Our results indicate than San 52 Jeronimo Island has the potential for red abalone mariculture and that this strategy may be a 53 useful tool in developing climate-resilient abalone restoration solutions aimed at bolstering 54 seafood production.

55 Introduction 56 Rising sea surface temperature and the increased frequency and severity of storms are 57 stressors for the growth of mariculture around the world (Barange & Perry, 2009). This 58 increases are serious concerns for the development of the abalone aquaculture industry. 59 Wild abalone fisheries have decreased significantly in the past decades, from 20,000 metric 60 tons (mt) in the 1970s to only about 6500 mt in 2016/17 (Cook, 2019). Hence, the current 61 worldwide abalone production has drastically changed to farming, from 50 mt in the 1970s 62 to 160,987 mt in 2016/17 (Cook 2016, 2019). A promising solution to reduce the impact of 63 fisheries is the development of conservation and management actions that diversify 64 production activities, such as aquaculture and mariculture. Indeed, aquaculture is 65 highlighted as a potential solution to the problem of food availability and security in the 66 United Nations 2030 Agenda (UN, 2018).

67 In Mexico, one of the most economically and culturally important fisheries is abalone. The 68 abalone fishery takes place on the Pacific coast of the Baja California Peninsula in the 69 states of Baja California and (Morales-Bojórquez et al., 2008). Even if 70 the worldwide trend is an increase in abalone aquaculture rather than harvesting wild 71 populations, in Mexico, the wild abalone fisheries produce ten times more volume than its 72 aquaculture industry (300 vs 23.5 tm/year; Cook, 2019). Although abalone catches in recent 73 years are less than 5% of its historical maximum, the fishery continues to be economically 74 important throughout the Baja California Peninsula (Guzmán-Del Próo et al., 2013, 2017). 75 However, along the entire coast, fishing has deteriorated due to a combination of multiple 76 stressors such as overfishing, diseases, extreme warming events and hypoxia (Micheli et 77 al., 2012; Ben-Horin et al., 2016; Boch et al., 2018; Sanford et al., 2019). These new 78 oceanic conditions resulted in landings of less than 100 mt from 2012 onwards in the state 79 of Baja California (northern state of the Peninsula) (DOF, 2018). This decline suggests that 80 additional conservation and management actions are needed for the recovery of natural 81 populations. The “National Abalone Rescue” program currently promoted by the Mexican 82 Ministry of Fisheries (INAPESCA) highlights that aquaculture is a strategy that could be 83 used to promote population conservation (DOF, 2018). And therefore, there is an 84 opportunity to develop abalone aquaculture programs in Mexico, to support conservation 85 programs. 86 87 In Ensenada, Baja California, red abalone mariculture has been carried out in the past in 88 different areas. In 1990, Searcy-Bernal and Salas-Garza (1990) conducted the first 89 experimental mariculture project to growth red abalone, H. rufescens , in floating cages in 90 Todos Santos Bay. Around the same years, a commercial red abalone mariculture company 91 "Abulones Cultivados" was established in the vicinities of Todos Santos Island (Preece & 92 Mladenov, 1999). However, the company moved to land-based facilities and still operating 93 until now in the area of Ejido Erendira, as the cost and operation for mariculture activities 94 in those years were high (Searcy-Bernal et al., 2010). More recently, Zertuche-González et 95 al. (2014) evaluated the growth performance of red abalone in an integrated multi-trophic 96 aquaculture (IMTA) farm, for one year, in the San Quintin Bay area. This study proves the 97 feasibility to growth out red abalone juveniles in the sea with an alternative fresh diet 98 (Ecklonia arborea). Now, we know more about the Oceanography of the area and we have 99 better technology to do mariculture. In addition, fishing cooperatives have greater work 100 capacity and the mentality towards aquaculture has been changing over time, due to wild 101 resources scarcity. Hence, we are at an ideal moment to carry out mariculture experiments 102 with the intention of enhancing marine resources in Baja California. 103

104 In the northeastern Pacific, abalone farms typically use the giant kelp Macrocystis pyrifera 105 harvested from the wild as feed (Evans & Langdon, 2000; García-Esquivel & Felbeck, 106 2009). However, in the last two decades extreme temperature and wave events, such as 107 ENSO and marine heatwaves, have substantially affected giant kelp in Baja California 108 (Ladah et al., 1999; Arafeh-Dalmau et al., 2019; Cavanaugh et al., 2019). Hence, it is 109 important to explore the effect of other macroalgae as an alternative abalone food source, to 110 cope with future regional giant kelp population variability. For example, the palm kelp E. 111 arborea is capable of surviving in relatively warm waters (>20º C) with low nutrients 112 where other kelps cannot survive (Hernández-Carmona et al., 2000, 2001; Zertuche- 113 González et al., 2014). On the other hand, storms, hypoxia and heatwaves events can affect 114 mariculture systems. One option against this is to move the cages vertically in the water 115 column and be able to submerge them during these events. Mariculture can increase fishers’ 116 communities’ ability to adapt to these changes by reducing the pressure on wild-caught 117 animals while promoting conservation alternatives to help the restoration of natural 118 populations. 119 120 Wild abalone populations have declined in Mexico and there is now uncertainty in recovery 121 due to climate change impacts on mariculture/restoration production in Baja California. To 122 test the potential for abalone mariculture in San Jeronimo Island, Baja California, Mexico, 123 we explored the feasibility of growing red abalone in cages attached to a long-line system. 124 Specifically, we examined 1) the effect of depth, surface and bottom (5 m), and 2) the 125 effect of three different brown macroalgae diets in the growth and survival of red abalone 126 juveniles. Lowering cages in the water column and reducing M. pyrifera are two strategies 127 which could bolster mariculture under ocean warming conditions in the region but which 128 require rigorous testing. 129 130 Materials and methods

131 Experimental study area

132 The study was carried out at San Jeronimo Island located in Ensenada Municipality in the 133 state of Baja California, Mexico (Fig. 1; 29° 47'34.9 "N, 115° 47'31.9" W), which is 1.3 km 134 long and 500 m wide. The marine resources of this area are under the concession of the 135 fishing cooperative "Sociedad Cooperativa de Producción Pesquera Ensenada, S.C.L.", 136 which participate actively in this research. The red abalone juveniles were obtained from 137 the commercial farm "Abulones Cultivados S. de R.L. de C.V." based 250 km north from 138 the study area. The abalone were transported from Ejido Eréndira to San Jeronimo Island in 139 coolers with a wet sponge base. After arriving, the organisms were gradually acclimated to 140 the seawater temperatures of the area and were kept in cages at sea at 14.98 °C (± 0.74 °C) 141 feeding with fresh brown macroalgae M. pyrifera ad libitum for a month before the 142 experiment started.

143

144 Experimental design 145 An experimental mariculture system was designed to assess the effect of different rearing 146 conditions (depth and diet) on the growth and survival of juvenile red abalone H. rufescens.

147 The experimental mariculture system consisted of plastic-coated metal mesh cages, 148 wrapped with ½ cm plastic “Vexar” mesh hanged from a 100 m long-line. The long line 149 was made of polistrong rope with two 20 m ropes to the anchoring system, which consists 150 of 3” diameter and 1.5 m long iron pipes that will be buried in the seabed at an angle of 151 approximately 45 °. Buoys (200 l drums with pressurized air) were placed at the ends of the 152 long line from the anchoring system and distributed along the flotation line. Eight cages 153 (0.80 X 0.80 X 0.36 m) were attached to the long-line, four in the surface and four at the 154 bottom (5 m). In each cage, three Australian baskets (0.75 X 0.25 X 0.20 m) were placed 155 (Fig. 2). So, a total of 24 Australian baskets were used for the experiment design (2 depths 156 x 3 diets). Additionally, to increase the available surface for the abalone, Australian baskets 157 were modified with the inclusion of a plastic plate in the middle (Supplementary material). 158 A total of 2,100 juveniles red abalone with an average shell length of 32 mm (± 3.33 mm) 159 were randomly divided into the 24 modified Australian baskets, so each basket had an 160 average of 87-104 abalone, with a density of 102-122 organisms m-2 as recommended by 161 Viera et al. (2014). Fifteen abalone per Australian basket, being 360 total (»17%), were 162 tagged with shellfish tags (Floy Tag & Mfg., Inc.). In each cage, one Thermo-sensors 163 HOBO U22 Temp Pro V2 was installed, so the temperature (°C) was recorded every half 164 hour.

165 As mentioned before, abalone were exposed to two different depth treatments, one at the 166 surface and one at the bottom (5 m). In the bottom treatment, cages were attached to the 167 long-line but submerged and laid on the sand with rocks at the bottom in each of the 168 corners. The effect of diet was also evaluated, and abalone were fed with three different 169 diets based on the most abundant brown macroalgae around the mariculture area. The first 170 diet tested was 100% giant kelp Macrocystis pyrifera (Mp), the second diet was 100% palm 171 kelp Ecklonia arborea (Ea) and the third diet consisted in a mix of 50% elk kelp 172 Pelagophycus porra and 50% giant kelp Macrocystis pyrifera (Pp/Mp). At the surface 173 cages, two cages were fed with giant kelp MpP, one cage with palm kelp Ea and one cage 174 with the mixed diet Pp/Mp. We repeated this design in the bottom cages. The harvest of E. 175 arborea was performed by SCUBA diving, the canopy of M. pyrifera was taken from the 176 boat and, P. porra rafted into the long line system and was harvested from it. Abalone were 177 fed ad libitum once per week, and the excess of macroalgae was removed when 178 needed. The experiment ran for three months (90 days), from March to June 2019.

179 Red abalone growth

180 The abalone growth of the 360 tagged red abalone was measured one a month in a period of 181 three months (90 days) culture. The growth was assessed by measuring the abalone shell 182 length (SL, mm) monthly. To measure shell length, we used a digital caliper (Mitutoyo 183 Absolute AOS CD 6”AX) with an accuracy of ± 0.01 mm. For survival we counted 100% 184 of the abalone in the experiment (initial n=2100).

185 Statistical analysis

186 All statistical analyses were performed with STATISTICA v. 12 software. To test for 187 differences in abalone growth among treatments, we executed a two-way ANOVA. We 188 considered total abalone growth (mm) at the end of the trial and the shell length at each 189 measurement date as the dependent variables. The depths and diets treatments as our 190 independent variables. Levene's F-test was used to assess the homogeneity of variances 191 (Brown & Forsythe, 1974).

192

193 Results

194 The experiment lasted three months (90 days) and the red abalone, Haliotis rufescens, mean 195 daily increment in shell length (DISL) was 87 ± 13 µm d-1. The mean total growth (TG) in 196 shell length was 7.86 ± 1.13 mm and the average monthly growth rate (MGR) was 2.62 ± 197 0.4 mm/month (ranging from 1.9 to 3.1 mm/month). The final survival rate of all was 97%.

198

199 Depth effect on red abalone growth and survival

200 Abalone from the surface cages had an average daily increment in SL of 93 ± 12 µm d-1 and 201 for the bottom cages 82 ± 13 µm d-1. On average, the abalone from the surface cages grew 202 more during the experimental period than the abalone from the bottom cages (8.33 ± 1.06 203 vs. 7.38 ± 1.13 mm of total period growth, and from 2.8 ± 0.4 vs. 2.5 ± 0.4 mm of monthly 204 growth rate). However, there were no statistically significant differences in the growth

205 parameters from surface and bottom cages (Fig. 3, two-way ANOVA, F1,4=3.066, p= 206 0.155).

207

208 Diet effect on red abalone growth and survival

209 Daily increment in shell length in abalone fed with a 100% of M. pyrifera was 88 ± 10 µm 210 d-1, 7.94 ± 0.88 mm of TG during the experiment period and 2.6 ± 0.3 mm/month in 211 average MGR. With the diet of a 100% E. arborea abalone grew 99 ± 7 µm d-1 of DISL, 212 8.86 ± 0.62 mm of TG and 3.0 ± 0.2 mm/month in average MGR. Abalone fed a mixed diet 213 of 50% M. pyrifera and 50% Pelagophycus porra grew 74 ± 13 µm d-1, 6.68 ± 1.19 mm 214 and 2.2 ± 0.4 mm/month of DISL, TG and MGR (Fig. 4). Details are in Table 1. As before, 215 no statistically significant differences in the growth parameters were found among diet

216 treatments (Fig. 4, two-way ANOVA, F2,4=4.120, p= 0.107).

217

218 Temperature

219 The temperature (°C) was recorded every half hour during the length of the experiment 220 (Fig. 5). For the surface treatment, the mean temperature was 13.69 ± 0.92 °C (Max= 221 18.62; Min= 12.01). For the bottom treatment, we recorded a mean temperature of 14.01 ± 222 0.94 °C (Max=17.85; Min=12.01). So, using daily means there were no statistically 223 significant differences in the temperature between the surface and the bottom (ANOVA, 2 224 R =0.007, F1,270=0.88, p=0.41).

225

226

227 Discussion

228 Depth effect on red abalone growth and survival 229 We tested the effect of the depth on the growth and survival of the red abalone, as a 230 potential solution for climate changes such as sea surface warming and storms. There were 231 no statistically significant differences in growth between the depth treatments (Fig. 3). 232 Temperature was similar between treatments (Fig. 5), so the slight increase observed in 233 growth at the surface may have been related to other variables such as dissolved oxygen, 234 pH, light availability, currents or turbidity (Morash & Alter, 2015). We also recorded more 235 sediment in the bottom cages and this could have affected the little differences observed in 236 the monthly growth rate and survival observed between depths of 2.8 vs. 2.5 mm/month 237 and 99% vs. 95% survival in surface and bottom treatments, respectively. However, our 238 results indicate that during adverse climate events in the area it will be possible to lower the 239 cages to protect the abalone and the infrastructure.

240

241 Diets effect on red abalone growth and survival

242 In our experiment, we found that red abalone H. rufescens grew better with E. arborea (99 243 µm d-1; 3 mm/month) than with M. pyrifera (88 µm d-1; 2.6 mm/month) or M. pyrifera 244 mixed with P. porra (75 µm d-1; 2.2 mm/month). In contrast, Zertuche-Gonzalez et al. 245 (2014) in the same region found a slightly better growth on red abalone, of similar size (20 246 mm) fed with M. pyrifera (2.5 mm/month) than those fed with E. arborea (2.2 247 mm/month), being this difference between fresh diets more evident in terms of the final 248 weight reached (24.9 vs. 18.6 g of final weight, respectively). Although there were no 249 statistical differences in the growth parameters related to shell length measures. Differences 250 between these two studies can be related with oceanography differences between culture 251 sites, being San Jeronimo Island a more dynamic ambient with cooler water temperatures 252 (12-18.6 °C), whereas San Quintin Bay is a moderate hypersaline coastal lagoon with 253 warmer temperatures reaching up to 21.5 °C at the mouth to 27.5 °C at the head (Alvarez- 254 Borrego & Alvarez-Borrego, 1982). Differences in monthly growth rates can also be related 255 to seed quality, temperature regime during culture and the species-specific thermal 256 preferred and optimum for growth. Díaz et al. (2000) found that juvenile red abalone of 46- 257 59 mm had a preferred temperature of 18.8°C whereas the optimum temperature for growth 258 was 18.4 °C, when abalone were acclimated to 17 °C (Díaz et al., 2000). Later, Steinarsson 259 & Imsland (2003), reported an optimal temperature for growth of 16.5 °C for 21 mm red 260 abalone and 17.2 °C for 25-66 mm, when acclimated at 15 °C. Moreover, macroalgae 261 morphotypes and proximal composition can vary between sites related to the oceanographic 262 conditions as currents, water motion, temperatures, light and nutrients (Roberson & Coyer, 263 2004; Demes et al., 2009; Landa-Cansigno et al., 2017).

264 Nevertheless, the viability for fishers to obtain M. pyrifera is much easier in time, money 265 and effort than to obtain E. arborea. This is because, E. arborea is underwater and to 266 acquire it SCUBA diving is need it, meanwhile, the canopy of M. pyrifera can be found in 267 the surface and be harvested from the boat. However, in the case of a future reduction in 268 wild population of M. pyrifera in Baja California due to extreme temperatures or other 269 environmental disturbances, our results suggest that the use of E. arborea (Fig. 4) is a 270 suitable alternative food source during ocean warming or storm impacts.

271 Growth rates in red abalone shell length fed with M. pyrifera range from 34 µm d-1 in 8 mm 272 SL (Trevelyan et al., 1998) to 73 µm d-1 in 20-60 mm SL (Zertuche-González et al., 2014). 273 The 88 µm d-1 growth registered in red abalone (32 mm SL) fed with M. pyrifera in this 274 study is promising. Our finding suggests the high potential this mariculture system has for 275 San Jeronimo Island based on M. pyrifera diet alone, currently the most dominating 276 macroalgae in the region. We examined alternatives to M. pyrifera algal diets for abalone 277 which could be used in Baja California during extreme temperature events (Ladah & 278 Zertuche, 1999; Cavanaugh et al., 2019). Some authors recommend the use of red algae, for 279 example, dulse Palmaria mollis to boost the red abalone growth (Evans & Langdon, 2000), 280 obtaining 124 µm d-1 in juvenile H. rufescens. This data is consistent with Guzman del Próo 281 et al. (2003) who remarks, that the natural diet of Haliotis genus of the Mexican Pacific 282 coast includes mainly red algae. In contrast, Leighton (1966) demonstrated that H. 283 rufescens had a distinct preference for brown algae, in particular, M. pyrifera and Eggregia 284 menziesii. Moreover, Poor (1972) studied the effect of diet in H. discuss hannai growth 285 rates and concluded that brown algae are more efficiently assimilated and promote greater 286 growth than red algae. Other studies use mixtures of brown algae, for example, Searcy- 287 Bernal & Salas-Garza (1990) obtained a 74 µm d-1 in H. rufescens fed with M. pyrifera and 288 E. menziesii. Abalone growth rates on natural diets are reported to range from 0.8 µm d-1 289 for H. iris (20 mm SL) fed Ulva lactuca (Stuart & Brown, 1994) to 139 µm d-1 for H. 290 discuss hannai (24–34 mm SL) fed Eisenia bicyclis (Uki et al., 1986). We have to continue 291 studying the effect of mix algae diets and their economic viability in mariculture systems. 292 Also, we have to consider that the feeding rate of abalone depends on body size, type of 293 food, density, and temperature (Capinpin et al., 1999; Nelson et al., 2002).

294 Temperature

295 Temperature is the main variable that controls the rate of most metabolic processes in 296 abalone (Morash & Alter, 2015). Outside their optimum range, individuals adjust basic 297 physiological functions to maintain basal metabolic demands (Medina-Romo et al., 2010).

298 Red abalone, H. rufescens, preferential temperature (Tpref) increases across development 299 until 30 mm shell length and then declines with further increasing shell length (Steinarsson

300 & imsland, 2003). The Tpref of H. rufescens is 18°C (Leighton, 1974, Diaz et al., 2000). 301 However, at 25°C H. rufescens begin to present detachment symptoms and the maximum 302 critical temperature is 27.5°C (Díaz et al., 2006). In this study, we registered a mean 303 temperature for the surface treatment, 13.69 ± 0.92 °C (Max= 18.62; Min= 12.01) and for 304 the bottom treatment 14.01 ± 0.94 °C (Max=17.85; Min=12.01). The temperature combined 305 with the growth and survival data indicates that San Jeronimo Island has a high potential 306 for red abalone mariculture. It is critical to have a robust understanding of the effect of 307 temperature on abalone metabolism and growth (Morash & Alter, 2015), to be able to 308 predict the future effects of rising ocean temperature on abalone farming.

309 Future directions/management/policy/conservation implications

310 Abalone aquaculture and mariculture projects have been very successful in several Asian 311 countries. Currently, about 150,000 tons of abalone is produced in China, South Korea and 312 Japan, equivalent to the 95% of world abalone production (Cook, 2016). Valuable insights 313 could be learned from these cases when adapting similar practices in México. For example, 314 in these countries, aquaculture activities are carried out under a joint collaborative scheme 315 between academia, private initiatives, local communities, and government agencies (Lee, 316 2019). In the context of application in Mexico, mariculture could, not only produce food 317 but also to diversify the activities of fishing communities to help restoration and 318 conservation projects enhance their resiliency to the impacts of climate change. 319 Acknowledgments

320 To the fishing cooperative “Ensenada” and the NGO “Comunidad y Biodiversidad A.C.” 321 (COBI) for their support. To the group “Monitoreo y Conservación de Especies” 322 (MOCOES) for their hard work. To Mex-Cal (www.mex-cal.org) for their time and effort. 323 This paper was prepared with funds provided by the “Universidad Autónoma de Baja 324 California” (UABC, , B.C., Mexico) and the National Council for Science and 325 Technology (CONACyT, CDMX, Mexico)”.

326

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