Global Change Biology Global Change Biology (2014) 20, 2108–2116, doi: 10.1111/gcb.12472
Carry-over effects of multiple stressors on benthic embryos are mediated by larval exposure to elevated UVB and temperature J E A N N I N E F I S C H E R and N I C O L E E . P H I L L I P S School of Biological Sciences and Coastal Ecology Laboratory (VUCEL), Victoria University of Wellington, P.O. Box 600, Wellington 6140, New Zealand
Abstract Damaging effects of UVB in conjunction with other stressors associated with global change are well-established, with many studies focused on vulnerable early life stages and immediate effects (e.g., mortality, developmental abnormalities). However, for organisms with complex life cycles, experiences at one life stage can have carry-over effects on later life stages, such that sublethal effects may mediate later vulnerability to further stress. Here, we exposed embryos in benthic egg masses of the New Zealand intertidal gastropod Siphonaria australis to treatments of either periodic stress (e.g., elevated UVB, salinity, and water temperature mimicking tidepool conditions in which egg masses are commonly found during summer) or control conditions (low UVB, ambient salinity, and water temperatures). Although there was high mortality from stressed egg masses, 24% of larvae hatched successfully. We then exposed the hatching larvae from both egg mass treatments to different combinations of water temperature (15 or 20 °C) and light (high UVB or shade) 12 h per day for 10 days. The most stressful larval conditions of 20 °C/high UVB resulted in low survival and stunted growth. Carry-over effects on survival were apparent for shaded larvae exposed to elevated temperature, where those from stressed egg masses had 1.89 higher mortality than those from control egg masses. Shaded larvae were also larger and had longer velar cilia if they were from control egg masses, independent of larval temperature. These results demonstrate that previous experience of environmental stress can influence vulnerability of later life stages to further stress, and that focus on a single life stage will underestimate cumulative effects of agents of global change. Keywords: benthic development, carry-over effects, gastropod, intertidal, invertebrate larvae, temperature, UVB Received 9 August 2013; revised version received 31 October 2013 and accepted 8 November 2013
Introduction Exposure to ultraviolet radiation (UVR), particularly the more harmful, shorter UVB wavelengths (280– 315 nm), can cause an array of deleterious impacts on aquatic organisms (reviewed by Hader et al., 2007; Llabres et al., 2013), with potential flow on effects through populations and communities (Bothwell et al., 1994; Chatila et al., 1999; Perin & Lean, 2004; Wahl et al., 2004). Ozone depletion has led to increased UVB radiation to the Earth for several decades (Kerr & McElroy, 1993; Weatherhead & Andersen, 2006) and, although ozone levels have been recovering since the enactment of the Montreal Protocol in 1989, complex interactions between ozone, other components of the atmosphere, and climate change, make future changes in UVB difficult to predict (McKenzie et al., 2011). Globally, UVB irradiance is not spatially uniform, such that ecosystems in some regions are more vulnerable than Correspondence: Nicole E. Phillips, tel. +644 463 5233, fax + 644 463 5331, e-mail: [email protected]
2108
others; for example, locations in the southern hemisphere can receive much greater mean and peak UV irradiance than similar northern latitudes (Seckmeyer & McKenzie, 1992; McKenzie et al., 2006; Seckmeyer et al., 2008). Furthermore, due to seasonal variability, in most temperate regions the maximum intensity of UVB generally occurs in summer, at a time that coincides with the escalation of biological processes in many ecosystems, e.g., growth, productivity, reproduction, species interactions (McKenzie et al., 1999). Environmental stressors such as UVR rarely act in isolation, instead often co-occurring with other anthropogenic or natural stressors, which can result in synergistic responses of affected organisms (Nystrom et al., 2000; Vinebrooke et al., 2004; Bancroft et al., 2008). The importance of shifting from examining effects of single stressors to multiple stressors on organisms is increasingly recognized, particularly in light of the complex components of global change and the high likelihood of interactive effects among them (Harley et al., 2006; Byrne, 2011). In marine systems, organisms in intertidal habitats are frequently © 2013 John Wiley & Sons Ltd
C A R R Y - O V E R E F F E C T S O F M U L T I P L E S T R E S S O R S 2109 subjected to simultaneous multiple stressors when low tide coincides with mid-day extremes of temperature and solar radiation (Helmuth et al., 2002). A common developmental strategy for aquatic taxa (including insects, amphibians, fish, and marine invertebrates) is the deposition of egg masses or capsules onto the benthos, where embryonic development occurs before the release of advanced larval stages. Encapsulated embryos developing in the intertidal have limited capacity to respond to stress due to immobility and physiological immaturity, and hatching larvae must spend additional days to weeks feeding in the water column, before finally settling to benthic habitat. Early life stages undergoing rapid and dramatic physiological change are particularly vulnerable to abiotic stressors (Pechenik, 1987), and previous work in Australia and New Zealand has demonstrated that high summertime UVR combined with other intertidal conditions (e.g., increased temperature, salinity, desiccation) results in high embryonic mortality in egg masses of several mollusc species (Przeslawski et al., 2005; Russell & Phillips, 2009a,b). In larval amphibians UVB interacts with pathogens, temperature, contaminants, and predator cues to increase mortality well above that which results from each stressor independently (Searle et al., 2010). For organisms with complex life cycles, not only can exposure to stress cause mortality or other direct damage to early life stages, but for those which survive, these early experiences often also results in legacy, or carry-over effects, later in life (Pechenik, 2006; Marshall & Morgan, 2011). Across a variety of species, nutritional, pollutant, or osmotic stress in the larval stage can lead to poor juvenile growth and survival, or reduced fitness for adults (Pechenik et al., 2001; Phillips, 2002, 2004; Ng & Keough, 2003). Although there is a growing literature on effects of UVR on early life stages, most work on invertebrates has only examined responses in one life stage (either on benthic embryos or planktonic larvae), and little is known about relative susceptibility of encapsulated embryos compared with planktonic larvae (Pechenik, 1999). Furthermore, larvae that have survived embryonic exposure to UVR and other stressors while encapsulated may have differential vulnerability to further exposure to stressors in the plankton, and effects of UVR exposure in the larval stage may be mediated by other co-occurring environmental variables such as water temperature. To the best of our knowledge, however, no studies have examined how survivors of sublethal UVR and other stressors during embryonic development in the egg mass cope with additional later stress as larvae in the water column. © 2013 John Wiley & Sons Ltd, Global Change Biology, 20, 2108–2116
Siphonaria australis is a marine gastropod that commonly deposits egg masses in intertidal habitats in New Zealand where embryos develop for approximately 1 week before hatching out as planktonic larvae. In summer, these encapsulated embryos are frequently subjected to extreme environmental conditions, including high UVB, with subsequent high embryonic mortality (Russell & Phillips, 2009a). Here, we used a laboratory experiment to examine how exposure to multiple, abiotic stressors (high UVB, temperature, and salinity; mimicking tidepool conditions at low tide in summer) in egg masses of S. australis mediates the performance of survivors during larval exposure to high UVB and elevated temperature in the water column.
Materials and methods
Egg mass treatments In January 2012, we collected adult Siphonaria australis from intertidal sites in the Wellington region of New Zealand (Princess Bay, 41°20′45.86′S 174°47′26.60′E) and brought them to the Victoria University Coastal Ecology Laboratory (VUCEL) where they were maintained in aquaria with constantly flowing filtered seawater (FSW; 10 lm mesh size). Rocks with algae were also collected from the intertidal sites and added to the aquaria to provide substrate and food. Aquaria were checked daily, and when six freshly deposited (
Carry-over effects of multiple stressors on benthic embryos are mediated by larval exposure to elevated UVB and temperature J E A N N I N E F I S C H E R and N I C O L E E . P H I L L I P S School of Biological Sciences and Coastal Ecology Laboratory (VUCEL), Victoria University of Wellington, P.O. Box 600, Wellington 6140, New Zealand
Abstract Damaging effects of UVB in conjunction with other stressors associated with global change are well-established, with many studies focused on vulnerable early life stages and immediate effects (e.g., mortality, developmental abnormalities). However, for organisms with complex life cycles, experiences at one life stage can have carry-over effects on later life stages, such that sublethal effects may mediate later vulnerability to further stress. Here, we exposed embryos in benthic egg masses of the New Zealand intertidal gastropod Siphonaria australis to treatments of either periodic stress (e.g., elevated UVB, salinity, and water temperature mimicking tidepool conditions in which egg masses are commonly found during summer) or control conditions (low UVB, ambient salinity, and water temperatures). Although there was high mortality from stressed egg masses, 24% of larvae hatched successfully. We then exposed the hatching larvae from both egg mass treatments to different combinations of water temperature (15 or 20 °C) and light (high UVB or shade) 12 h per day for 10 days. The most stressful larval conditions of 20 °C/high UVB resulted in low survival and stunted growth. Carry-over effects on survival were apparent for shaded larvae exposed to elevated temperature, where those from stressed egg masses had 1.89 higher mortality than those from control egg masses. Shaded larvae were also larger and had longer velar cilia if they were from control egg masses, independent of larval temperature. These results demonstrate that previous experience of environmental stress can influence vulnerability of later life stages to further stress, and that focus on a single life stage will underestimate cumulative effects of agents of global change. Keywords: benthic development, carry-over effects, gastropod, intertidal, invertebrate larvae, temperature, UVB Received 9 August 2013; revised version received 31 October 2013 and accepted 8 November 2013
Introduction Exposure to ultraviolet radiation (UVR), particularly the more harmful, shorter UVB wavelengths (280– 315 nm), can cause an array of deleterious impacts on aquatic organisms (reviewed by Hader et al., 2007; Llabres et al., 2013), with potential flow on effects through populations and communities (Bothwell et al., 1994; Chatila et al., 1999; Perin & Lean, 2004; Wahl et al., 2004). Ozone depletion has led to increased UVB radiation to the Earth for several decades (Kerr & McElroy, 1993; Weatherhead & Andersen, 2006) and, although ozone levels have been recovering since the enactment of the Montreal Protocol in 1989, complex interactions between ozone, other components of the atmosphere, and climate change, make future changes in UVB difficult to predict (McKenzie et al., 2011). Globally, UVB irradiance is not spatially uniform, such that ecosystems in some regions are more vulnerable than Correspondence: Nicole E. Phillips, tel. +644 463 5233, fax + 644 463 5331, e-mail: [email protected]
2108
others; for example, locations in the southern hemisphere can receive much greater mean and peak UV irradiance than similar northern latitudes (Seckmeyer & McKenzie, 1992; McKenzie et al., 2006; Seckmeyer et al., 2008). Furthermore, due to seasonal variability, in most temperate regions the maximum intensity of UVB generally occurs in summer, at a time that coincides with the escalation of biological processes in many ecosystems, e.g., growth, productivity, reproduction, species interactions (McKenzie et al., 1999). Environmental stressors such as UVR rarely act in isolation, instead often co-occurring with other anthropogenic or natural stressors, which can result in synergistic responses of affected organisms (Nystrom et al., 2000; Vinebrooke et al., 2004; Bancroft et al., 2008). The importance of shifting from examining effects of single stressors to multiple stressors on organisms is increasingly recognized, particularly in light of the complex components of global change and the high likelihood of interactive effects among them (Harley et al., 2006; Byrne, 2011). In marine systems, organisms in intertidal habitats are frequently © 2013 John Wiley & Sons Ltd
C A R R Y - O V E R E F F E C T S O F M U L T I P L E S T R E S S O R S 2109 subjected to simultaneous multiple stressors when low tide coincides with mid-day extremes of temperature and solar radiation (Helmuth et al., 2002). A common developmental strategy for aquatic taxa (including insects, amphibians, fish, and marine invertebrates) is the deposition of egg masses or capsules onto the benthos, where embryonic development occurs before the release of advanced larval stages. Encapsulated embryos developing in the intertidal have limited capacity to respond to stress due to immobility and physiological immaturity, and hatching larvae must spend additional days to weeks feeding in the water column, before finally settling to benthic habitat. Early life stages undergoing rapid and dramatic physiological change are particularly vulnerable to abiotic stressors (Pechenik, 1987), and previous work in Australia and New Zealand has demonstrated that high summertime UVR combined with other intertidal conditions (e.g., increased temperature, salinity, desiccation) results in high embryonic mortality in egg masses of several mollusc species (Przeslawski et al., 2005; Russell & Phillips, 2009a,b). In larval amphibians UVB interacts with pathogens, temperature, contaminants, and predator cues to increase mortality well above that which results from each stressor independently (Searle et al., 2010). For organisms with complex life cycles, not only can exposure to stress cause mortality or other direct damage to early life stages, but for those which survive, these early experiences often also results in legacy, or carry-over effects, later in life (Pechenik, 2006; Marshall & Morgan, 2011). Across a variety of species, nutritional, pollutant, or osmotic stress in the larval stage can lead to poor juvenile growth and survival, or reduced fitness for adults (Pechenik et al., 2001; Phillips, 2002, 2004; Ng & Keough, 2003). Although there is a growing literature on effects of UVR on early life stages, most work on invertebrates has only examined responses in one life stage (either on benthic embryos or planktonic larvae), and little is known about relative susceptibility of encapsulated embryos compared with planktonic larvae (Pechenik, 1999). Furthermore, larvae that have survived embryonic exposure to UVR and other stressors while encapsulated may have differential vulnerability to further exposure to stressors in the plankton, and effects of UVR exposure in the larval stage may be mediated by other co-occurring environmental variables such as water temperature. To the best of our knowledge, however, no studies have examined how survivors of sublethal UVR and other stressors during embryonic development in the egg mass cope with additional later stress as larvae in the water column. © 2013 John Wiley & Sons Ltd, Global Change Biology, 20, 2108–2116
Siphonaria australis is a marine gastropod that commonly deposits egg masses in intertidal habitats in New Zealand where embryos develop for approximately 1 week before hatching out as planktonic larvae. In summer, these encapsulated embryos are frequently subjected to extreme environmental conditions, including high UVB, with subsequent high embryonic mortality (Russell & Phillips, 2009a). Here, we used a laboratory experiment to examine how exposure to multiple, abiotic stressors (high UVB, temperature, and salinity; mimicking tidepool conditions at low tide in summer) in egg masses of S. australis mediates the performance of survivors during larval exposure to high UVB and elevated temperature in the water column.
Materials and methods
Egg mass treatments In January 2012, we collected adult Siphonaria australis from intertidal sites in the Wellington region of New Zealand (Princess Bay, 41°20′45.86′S 174°47′26.60′E) and brought them to the Victoria University Coastal Ecology Laboratory (VUCEL) where they were maintained in aquaria with constantly flowing filtered seawater (FSW; 10 lm mesh size). Rocks with algae were also collected from the intertidal sites and added to the aquaria to provide substrate and food. Aquaria were checked daily, and when six freshly deposited (
