J. Phycol. *, ***–*** (2020) © 2020 Phycological Society of America DOI: 10.1111/jpy.13000
EFFECTS OF HEAT WAVES AND LIGHT DEPRIVATION ON GIANT KELP JUVENILES (MACROCYSTIS PYRIFERA, LAMINARIALES, PHAEOPHYCEAE)1
Mariana Sanchez-Barredo #, Jose Miguel Sandoval-Gil2,# , Jose Antonio Zertuche-Gonzalez Instituto de Investigaciones Oceanologicas, Universidad Autonoma de Baja California, Ensenada, Baja California, Mexico Lydia B. Ladah Department of Biological Oceanography, CICESE, Ensenada, Baja California, Mexico Marıa Dolores Belando-Torrentes Instituto de Investigaciones Oceanologicas, Universidad Autonoma de Baja California, Ensenada, Baja California, Mexico Rodrigo Beas-Luna Facultad de Ciencias Marinas, Universidad Autonoma de Baja California, Ensenada, Baja California, Mexico and Alejandro Cabello-Pasini Instituto de Investigaciones Oceanologicas, Universidad Autonoma de Baja California, Ensenada, Baja California, Mexico
Due to climate change, the incidence of marine detrimental to juvenile survival, and therefore heat waves (MHWs) has increased, yet their effects recruitment success of M. pyrifera forests, than on seaweeds are still not well understood. Adult episodic thermal stress from MHWs. Macrocystis pyrifera sporophytes of , the species Key index words: heat waves; Juveniles; Macrocystis forming the iconic giant kelp forests, can be pyrifera; photoacclimation; physiology negatively affected by thermal stress and associated environmental factors (e.g., nutrient depletion, light Abbreviations: D, darkness; ETR, electron transport deprivation); however, little is known about the rate; L, Light; MHW, marine heat wave; NPQ, non- tolerance/vulnerability of juvenile sporophytes. photochemical quenching; RLC, rapid light curve Simultaneously to MHWs, juveniles can be subjected to light limitation for extended periods of time (days–weeks) due to factors causing turbidity, or In the framework of global climate change, a rise even because of shading by understory canopy- of seawater temperature (up to 3–4°C) is predicted forming seaweeds. This study evaluated the effects by the end of this century (IPCC 2013), and thus, of a simulated MHW (24°C, 7 d) in combination (or there is an increasing concern about the effects of not) with light deprivation, on the photosynthetic thermal stress on coastal biological communities, capacities, nutrient uptake, and tissue composition, such as seaweed beds (Smale et al. 2019). Macroal- as well as oxidative stress descriptors of M. pyrifera gae-dominated habitats provide critical ecological juvenile sporophytes (single blade stage, up to 20 cm and human services worldwide (Hurd et al. 2014). F F length). Maximum quantum yield ( v/ m)decreased Therefore, it is important to predict their response in juveniles under light at 24°C, likely reflecting some (tolerance, resilience) to thermal stress and the sub- damage on the photosynthetic apparatus or dynamic sequent impact on species-specific distribution pat- photoinhibition; however, no other sign of terns (Andrews et al. 2014, Smale et al. 2019, Straub physiological alteration was found in this treatment et al. 2019). (i.e., pigments, nutrient reserves and uptake, Exposure to high temperatures can lead to “dis- oxidative stress). Photosynthetic capacities were ruptive stress” in seaweeds, resulting from metabolic maintained or even enhanced in plants under light damage (Davison and Pearson 1996). Both experi- deprivation, likely supported by photoacclimation mental approaches and in situ observations have (pigments increment); by contrast, nitrate uptake and shown that the physiology of marine macrophytes internal storage of carbohydrates were strongly can be altered by exposure to high temperatures reduced, regardless of temperature. This study (Bruhn and Gerard 1996, Short et al. 2015, Mar ın- indicated that light limitation can be more Guirao et al. 2017). Generally, thermal stress can (i) alter enzymatic-mediated processes and cell mem- 1Received 28 October 2019. Accepted 15 March 2020. brane composition (Machalek et al. 1996, Los and 2Author for correspondence: e-mail [email protected]. Murata 2004), (ii) increase or decrease photosynthe- #These authors contributed equally to the manuscript. sis and growth depending on the duration and Editorial Responsibility: M. Edwards (Associate Editor)
1 2 MARIANA SANCHEZ-BARREDO ET AL. intensity of heat stress and its interaction with other M. pyrifera), and the influence of anthropogenic environmental factors (e.g., light, nutrients, UVB impacts (Holbrook et al. 2019, Smale et al. 2019). radiation; Kubler€ and Davison 1993, Bruhn and Ger- In Baja California, the influence of the California ard 1996, Brown et al. 2014, Xiao et al. 2015, Mabin Current and upwelling events provides the basic abi- et al. 2019), and (iii) result in photoinhibition, otic requirements (e.g., lower temperatures, nutri- increased respiration, and changes in pigment com- ents) for the development of M. pyrifera (Tegner position (Kubler€ and Davison 1993, Bruhn and Ger- and Dayton 1987). Conversely, thermal anomalies as ard 1996, Koch et al. 2007, Andersen et al. 2013). a consequence of episodic events such as ENSO, Heat stress has also been correlated with the pro- MHWs, or prolonged events such as the “Blob” (see duction of reactive oxygen species and increased Hu et al. 2017) can be correlated with damage or antioxidant capacity of intertidal seaweeds (Collen even complete disappearance of Giant Kelp forests, and Davison 1999, Cruces et al. 2012). Populations likely due to the cross-correlation of temperature near their distribution boundaries will most likely and other environmental factors, such as the deep- be more affected by thermal stress (Wernberg et al. ening of the thermocline and associated reduction 2011). of nutrients (North and Zimmerman 1984, Zimmer- There is evidence that short-term (days) thermal man and Robertson 1985, Ladah 2003, Schiel and anomalies of high intensity can be more harmful Foster 2015, Arafeh-Dalmau et al. 2019). Normal for submerged vegetation than persistent (but mod- summer warming causes reduced growth, bleaching erate) warming (Thompson et al. 2013, Wilson et al. and softening of tissues, increased epiphytation and 2015, Guerrero-Meseguer et al. 2017). The exposure death (North 1987); however, these effects can be to increasing annual maximum temperatures, the ameliorated by sub-thermocline nitrate influx fueled influence of marine heat waves (MHWs), or even by internal waves and mixing (Zimmerman and the influence of episodic/seasonal natural events Robertson 1985, Ladah et al. 2012). Ocean warming (e.g., ENSO) strongly affect macroalgae at regional and linked factors such as nutrient limitation can and local scales (Pacheco-Ru ız et al. 2003, Jord a restrict the distribution boundaries of kelp forests, et al. 2012, Schiel and Foster 2015). Even short-term as particularly observed along the coastline of Baja exposure to thermal stress may affect distribution California Peninsula (Ladah et al. 1999, Graham patterns, growth, and recruitment of seaweeds et al. 2007, Arafeh-Dalmau et al. 2019) and other (Andrews et al. 2014, Smale et al. 2019). coastal systems. As a result of climate change, short-term periods Despite the well-described negative effects of ther- of extreme temperature anomalies, such as longer mal stress on Macrocystis pyrifera forests (e.g., popula- and more severe summer MHWs, have increased tion dynamics, loss of canopy; North 1987, Ladah (Sch€ar and Jendritzky 2004, Perkins et al. 2012). et al. 1999, Cavanaugh et al. 2019), knowledge MHWs, often of short duration, can reduce repro- about the physiological mechanisms governing their duction and alter distribution of some seaweeds vulnerability and/or resilience is still limited (Brown (Andrews et al. 2014), and can promote mortality of et al. 2014), particularly at the juvenile stages. More- crustose coralline algae and local extinction of kelp over, M. pyrifera has a complicated alternation of communities (Short et al. 2015, Thomsen et al. generations in its life history, and juvenile stages 2019). The impact of MHWs on kelp forests may such as gametophytes and juvenile sporophytes may depend on the influence of latitudinal patterns of exhibit different resistance to environmental stres- genetic diversity, physiological versatility, and eco- sors (Manley and North 1984, Dean and Jacobsen logical resilience (Wernberg et al. 2018). Although 1986, Munoz~ et al. 2004, Ladah and Zertuche- understanding the effects of weather extremes (in- Gonz alez 2007, Mabin et al. 2019). Differences in cluding MHWs) on submerged vegetation has been the thermal tolerance of the various life history highlighted (Wernberg et al. 2012, 2016), seaweed stages of kelps can be decisive for the survival of a responses to thermal stress, such as physiological population (Graham 1996, Clarke 2003). Metabo- plasticity, tolerance, and resilience, remain poorly lism differs between the ontogenic stages of M. pyri- addressed to date in juvenile stages. fera (i.e., photosynthesis, light requirements; Dean The giant kelp, Macrocystis pyrifera, is a large kelp and Jacobsen 1986, Xu et al. 2015), similar to that forming some of the biggest and most productive indicated for other seaweeds (Xu et al. 2017). Also, temperate submerged vegetated ecosystems of the juvenile sporophytes of M. pyrifera lack the structural world, with relevant ecological and economic values complexity of adults, and consequently, they cannot (e.g., aquaculture, maintenance of water quality, rely on translocation of resources to cope with nursery and shelter for invertebrates, fishes, mam- stressful conditions (Graham et al. 2007). There- mals, and other algae; Reed and Brzezinski 2009, fore, acclimation responses and resistance to ther- Gordon and Cook 2013). The coastline of Baja Cali- mal stress would be expected to differ between fornia, Mexico, is considered among the regions adults and juveniles. particularly vulnerable to MHWs, due to the high The differential interaction of adults and juveniles levels of biodiversity, the prevalence of important with changing environmental factors that can occur kelp species at their warm boundaries (such as simultaneously with thermal stress, such as light GIANT KELP UNDER HEAT WAVES AND LIGHT DEPRIVATION 3 availability, can represent another potential source hypothesis of this study was that MHWs and light of variation of the responses to heat stress. For deprivation can induce physiological changes in instance, increased turbidity due to storm waves, juvenile sporophytes, and the metabolic integration coastal runoff, or even phytoplankton blooms can of these responses can be decisive to their tolerance dramatically reduce incident irradiance (near dark- and/or vulnerability to those combined stressors. ness) for weeks on the benthos (Dean and Jacob- Photosynthesis, bio-optical properties, nutritional sen 1984, Dean 1985, Cabello-Pasini et al. 2002, status, oxidative stress descriptors, and nitrate Schiel and Foster 2015). Phytoplankton blooms uptake rates were evaluated. As far as we know, commonly resulted for the combination of rising there is no background information about the inte- of seawater temperature and upwelled nutrients in gration of such physiological descriptors of M. pyri- spring–summer, and can lead to drastic reductions fera juveniles under the combination of disruptive of irradiance during weeks (less than 0.5 mol pho- (heat) and limitation (light deprivation) stressful tons m 2 d 1) in shallow bottoms near giant conditions. kelp forests (Dean and Jacobsen 1984). Also over- growth of canopy-forming seaweeds in later-spring/ early-summer at the edges of Macrocystis pyrifera MATERIALS AND METHODS populations, like the invasive Sargassum horneri, Sar- Collection of juvenile sporophytes. In September 2017, juve- gassum muticum, and Undaria pinnatifida that have nile sporophytes (single blade stage, up to 20 cm length) colonized progressively new coastal areas on the were collected along the edges of a healthy and dense (~0.3 Pacific coast of North America, can comprise light stipes m 2) Macrocystis pyrifera forest growing at 7–10 m availability for the development of juvenile stages depth in Bah ıa Todos Santos, Baja California, Mexico ° 0 ″ ° 0 ″ and recruitment (Ambrose and Nelson 1982, (35 54 21.90 N, 116 45 12.05 W). Surface seawater tempera- ture in this region ranges between 12 and 20°C, although it Schiel and Foster 2015, South et al. 2017). The can increase up to 4°C above the long-term mean during canopy of M. pyrifera adults and understory cano- ENSO and MHWs (Hern andez de la Torre et al. 2004, Leis- pies of other seaweeds (e.g., kelps species such as ing et al. 2015). Laminaria and Pterygophora) can also shade juve- During collection, algae were kept in black plastic bags to niles of M. pyrifera (North 1994). While adult avoid exposure to excessive sunlight. Within 2 h after collec- plants can counterbalance light limitation by both tion, juveniles were transported in large coolers filled with photoacclimation of deeper blades and transloca- seawater to the Marine Botany Lab at the University of Baja California. Juveniles were kept in 1-m3 outdoor tanks until tion of resources from apical parts of the fronds the beginning of the experiment, at averaged values of field reaching the sea surface (Manley and North 1984, temperature and light, 16°C and 6.6 mol photons m 2 Colombo-Pallota et al. 2006), young juveniles must d 1, respectively. Temperature was adjusted by using chillers, depend on their photosynthetic plasticity to sur- while the tanks were covered with plastic meshes to adjust vive. Light deprivation results in lower availability light to field values. Temperature was recorded at the collec- to metabolic energy needed to incorporate and tion site during the previous weeks using HOBO MX2202 assimilate inorganic carbon, and thus, in a drop in (ONSET, Bourne, MA, USA) data loggers. Light values were obtained by using a spherical 4p underwater quantum sensor photosynthate production (Hanelt and Lopez- attached to a data logger (LI-192 and LI-1500; LI-COR Bio- Figueroa 2012). Since the assimilation of inorganic sciences, Lincoln, NE, USA), and HOBO MX2202 data log- nitrogen into organic compounds requires energy gers calibrated against 2p quantum sensor LI-190R (LI-COR and carbon skeletons from photoassimilates, light Biosciences). limitation can lead to the alteration of the plant Experimental setup and design. After a 4 d acclimation per- N-metabolism, including N-uptake rates (Hurd iod, Macrocystis pyrifera juveniles were transplanted to 10-L et al. 2014). Changes in the bio-optical properties plastic transparent containers (nine juveniles per container) filled with filtered (1 lm) UV-irradiated seawater and aer- of photosynthetic tissues (e.g., absorptance) and ated. Each container was considered as an experimental unit pigments content are among the photoacclimation (EU), and all the EUs were placed within large incubators mechanisms which can be activated to optimize (VWR, model 2015 2015-2), which allowed for the control of light harvesting in seaweeds, including M. pyrifera light and temperature. Within the incubators, temperature juveniles (Umanzor et al. 2019). Compared to was adjusted to 16 and 24°C, corresponding to the averaged adult sporophytes, photoacclimation strategies of field values at the collection site and maximum values recorded during MHWs, respectively. A control light treat- juveniles are still poorly understood (Mabin et al. ment was also adjusted at 180 lmol photons m 2 s 1, pho- 2019, Umanzor et al. 2019). toperiod 12:12 h light:dark; this light corresponded to the The purpose of the present study was to evaluate averaged maximum irradiances measured at the collection the combined effects of a simulated MHW and light site at midday (from 90 to 300 lmol photons m 2 s 1), deprivation on juvenile sporophytes of Macrocystis and can be saturating for the photosynthesis of juvenile sporophytes (Umanzor et al. 2019). Other juveniles were kept pyrifera. An orthogonal design was used, based on – l 2 1 the exposure of juveniles to two temperatures (16 in almost darkness (5 10 mol photons m s ) by cover- ing the EUs with black plastic mesh. This low light condition, and 24°C) and two light conditions (saturating irra- 2 1 which is below compensation irradiance for photosynthesis diance ~180 lmol photons m s , and a light of juveniles (Umanzor et al. 2019), was selected following below compensation irradiance for photosynthesis, Dean and Jacobsen (1984) and Cabello-Pasini et al. 5–10 lmol photons m 2 s 1). The main (2002) who reported light values close to zero (0–0.5 mol 4 MARIANA SANCHEZ-BARREDO ET AL.