DETERMINING THE EXTENT TO WHICH WEATHER-RELATED ABIOTIC FACTORS INFLUENCE DAILY VARIATION IN EARLY BENTHIC PHASE MORTALITY OF INTERTIDAL MARINE INVERTEBRATES by Brittany Teresa Jenewein B.Sc. Thompson Rivers University, 2009 A thesis submitted in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE in Environmental Science in the Department of Biological Sciences Thesis examining committee: Dr. Louis Gosselin (PhD), Associate Professor and Thesis Supervisor, Department of Biological Sciences Dr. Brian Heise (PhD), Associate Professor, Chair, and Committee Member, Department of Natural Resource Science Dr. Donald Noakes (PhD), Full Professor and Committee Member, Department of Mathematics and Statistics Dr. Heather Hunt (PhD), External Examiner, Department of Biology, University of New Brunswick © Brittany Teresa Jenewein, 2013 Thompson Rivers University All rights reserved. This thesis may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. ii Thesis Supervisor: Associate Professor Dr. Louis Gosselin ABSTRACT Populations of marine intertidal invertebrates vary substantially in abundance from year to year. These differences might be partly due to cohorts experiencing 60 – 99% mortality during the first few days after the transition from pelagic to benthic environments. However, the causes of this mortality, including the role of weather conditions experienced during low tide, are not well understood. This study aimed to improve our understanding of the influence of low tide environmental stress on survival through the early benthic phase by (1) determining the influence of temperature and desiccation stress on mortality of newly settled mussels and the ontogeny of sensitivity to these stresses through the early benthic phase; (2) examining the mortality of barnacle cyprids from settlement to metamorphosis and mortality of early juveniles up to the age of 10 days after metamorphosis; and (3) documenting the frequency of occurrence of lethal conditions occurring in the field at low tide during the recruitment season. Laboratory experiments revealed that newly settled Mytilus trossulus of 1-2 mm shell length experienced a temperature tolerance threshold at 34°C and a desiccation tolerance threshold at a vapour pressure deficit level of 1.01 kPa. Mussels became highly tolerant to desiccation stress when they reached a size of 3 mm shell length, suggesting a size threshold of desiccation tolerance between 2-3 mm shell length. This size closely corresponds to the size at which some studies have reported juvenile M. trossulus relocate from protective filamentous algal habitat to adult habitat, suggesting ontogenetic shifts in habitat use by juvenile M. trossulus may be a response to changing vulnerability to desiccation stress. A field survey of Balanus glandula recruitment revealed that cyprid and juvenile mortality varied greatly among daily cohorts and was significantly higher under Fucus spp. cover than on bare surfaces. Contrary to expectations, cyprid mortality was not significantly influenced by weather-related abiotic conditions. This was likely due to the iii study being conducted during a La Niña cycle that may have had lower temperature and desiccation stress than is typical for Barkley Sound. Intertidal temperatures above the threshold tolerance levels for newly settled mussels were uncommon during the recruitment season, suggesting that temperature stress is not likely an important factor influencing early benthic phase mortality of mussels. The desiccation stress threshold level for newly settled mussels was frequently exceeded for several hours during the recruitment season, however, suggesting that desiccation stress may be an important factor influencing early benthic phase mortality in mussels that settle on open surfaces. In contrast, cyprid mortality on bare surfaces was not significantly influenced by desiccation stress or any other weather-related abiotic factors. I concluded that the survival of newly settled mussels likely depends upon the presence of protective microhabitats created by filamentous and fucoid algae, whereas barnacles experience reduced survival through the early benthic phase in the presence of fucoid algae. Changes in survival of these algae due to climate change could therefore have extensive influence on mortality through the early benthic phase and may subsequently affect population and community structure. Keywords: early post-settlement mortality; mortality factors; ontogenetic shift; physiological stress; marine invertebrates; desiccation; temperature; climate change iv TABLE OF CONTENTS Abstract .......................................................................................................................... ii Table of Contents .......................................................................................................... iv Acknowledgements ....................................................................................................... vi List of Figures .............................................................................................................. vii List of Tables ................................................................................................................. ix Chapter 1: General Introduction ....................................................................................... 1 LITERATURE CITED ....................................................................................... 4 Chapter 2: Ontogenetic shift in stress tolerance thresholds of the mussel Mytilus trossulus: Do low tide temperature and desiccation stress influence early benthic phase mortality? ........................................................................................................................ 7 INTRODUCTION .................................................................................................. 7 METHODS ............................................................................................................ 9 Study site ......................................................................................................... 9 Abiotic conditions in the intertidal zone ......................................................... 10 Sensitivity to temperature stress ..................................................................... 11 Sensitivity to desiccation stress ...................................................................... 13 Ontogeny of desiccation tolerance ................................................................. 14 Data analysis ................................................................................................. 14 RESULTS ............................................................................................................ 15 Abiotic conditions in the intertidal zone ......................................................... 15 Sensitivity to temperature stress ..................................................................... 20 Sensitivity to desiccation stress ...................................................................... 23 Ontogeny of desiccation tolerance ................................................................. 25 DISCUSSION ...................................................................................................... 26 Sensitivity to temperature stress ..................................................................... 26 Sensitivity to desiccation stress ...................................................................... 28 Ontogeny of desiccation tolerance ................................................................. 29 LITERATURE CITED ......................................................................................... 32 v Chapter 3: Is daily variation in early benthic phase mortality of the barnacle Balanus glandula influenced by low tide weather conditions or Fucus spp. cover? ...................... 37 INTRODUCTION ................................................................................................ 37 METHODS .......................................................................................................... 39 Study site and organism ................................................................................. 39 Weather-related abiotic conditions in the upper intertidal zone ...................... 40 Daily settlement, cyprid mortality, and juvenile mortality .............................. 41 Effect of weather-related abiotic conditions on cyprid mortality..................... 42 Effect of Fucus cover on settlement and mortality of cyprids and juveniles .... 42 RESULTS ............................................................................................................ 43 Weather-related abiotic conditions in the upper intertidal zone ...................... 43 Daily settlement, cyprid mortality, and juvenile mortality .............................. 45 Effect of weather-related abiotic conditions on cyprid mortality..................... 48 Effect of Fucus cover on settlement and mortality of cyprids and juveniles .... 51 DISCUSSION ...................................................................................................... 55 Weather-related abiotic conditions in the upper intertidal zone ...................... 55 Daily settlement, cyprid mortality, and juvenile mortality .............................. 55 Effect of weather-related abiotic conditions on cyprid mortality..................... 56 Effect of Fucus cover on settlement and mortality of cyprids and juveniles .... 58 Conclusions ................................................................................................... 58 LITERATURE CITED ......................................................................................... 60 Chapter 4: General conclusion ....................................................................................... 65 SUMMARY OF RESULTS ................................................................................. 65 CONCLUSIONS AND FUTURE DIRECTIONS ................................................. 67 LITERATURE CITED ......................................................................................... 69 Appendix A. Autocorrelation analysis of multiple regression models predicting intertidal relative humidity and intertidal temperature on bare surfaces. ........................................ 71 Appendix B. Intertidal temperature and relative humidity conditions during low tide at Grappler Inlet ................................................................................................................ 73 vi ACKNOWLEDGEMENTS I would first like to thank my supervisor, Dr. Louis Gosselin, for his endless support, guidance, and motivation provided throughout the duration of this project. I also thank my committee members, Dr. Brian Heise, Dr. Donald Noakes, and Dr. Heather Hunt, for their support of this project. There are many people who worked at the Bamfield Marine Sciences Centre (BMSC) during my stay who deserve a great deal of thanks. The maintenance staff, Cliff Haylock and Jack Radoslovich, helped with construction of my weather station and graciously lent me their tools. John Richards and Janice Pierce were a tremendous help when I encountered problems with my boat. Beth Rogers and Dr. Dave Riddell always knew exactly what and where to get the supplies I needed. And of course, I would like to extend an immense amount of gratitude to all of my field assistants: Nicole Straughan, Christine Hansen, Emily Kehoe, Shirley Coulson, Marissa Webber, David Minkley, Travis Tai, Annie Livingstone, and Phil Lavoie. I thank everyone else at BMSC who made living in a remote location for seven months a joyful experience. I extend extra thanks to Christine Hansen for answering hundreds of questions and providing me with great advice as I followed in her footsteps. Finally, I thank all of my friends and family for their continued support. This research was funded by a National Science and Engineering Research Council Strategic Project Grant to LA Gosselin (STPSC 357084). I was supported by a Robert Frazier Memorial Fellowship (Thompson Rivers University) and a John Boom Memorial Scholarship (Bamfield Marine Sciences Centre). Permits in place for this research included: a DFO animal collection permit (XR 141 2010, XR 82 2011), Thompson Rivers University AUP (2010-10, 2011-09R), Bamfield Marine Sciences Centre AUP (RS-10-22, RS-11-13), and Huu-Ay-Aht First Nations heritage investigation permits (HFN 057-10, HFN 008-11). vii LIST OF FIGURES Figure 2.1. (A) Actual maximum daily mid-intertidal temperatures (°C) and (B) predicted maximum daily mid-intertidal VPD at the rock surface for May to August, 2011.. ......... 16 Figure 2.2. Temperature (°C) and vapour pressure deficit (kPa) data collected at 3 intertidal heights on Wizard Islet on 6 September 2012.. ................................................ 18 Figure 2.3. Differences in rock surface colour at A) 2.5 m and B) 2.75 m above MLLW. ......................................................................................................................... 20 Figure 2.4. Effect of prolonged exposure to various temperature treatments on mortality of newly settled (1-2 mm SL) mussels. .......................................................................... 21 Figure 2.5. Number of days during the 2010 and 2011 settlement seasons when the intertidal rock surface temperature near the upper limit of adult mussel distribution exceeded 33°C for different durations at low tide.. ......................................................... 22 Figure 2.6. Effect of prolonged exposure to various vapour pressure deficits (kPa) on mortality of juvenile (1-2 mm SL) mussels (Mytilus trossulus). ..................................... 23 Figure 2.7. Number of days during the 2011 settlement season that vapour pressure deficit was ≥ 1.01 kPa (mussel threshold) for different durations during low tide. .......... 24 Figure 2.8. Weight of water (g) contained within tufts of Cladophora columbiana after 8 h aerial exposure as a function of the blotted dry weight (g) of the algae ..................... 25 Figure 2.9. Effect of relative humidity on mortality of mussels within different size classes. .......................................................................................................................... 26 Figure 3.1. (A) Predicted maximum daily mid-intertidal temperatures (°C) and (B) predicted maximum daily mid-intertidal VPD at the rock surface for May and June 2011. ............................................................................................................................. 44 Figure 3.2. Weather conditions experienced by each cohort of Balanus glandula on bare surfaces during the first 2 d after settlement. (A) Cumulative predicted intertidal temperature (°C). (B) Cumulative predicted intertidal VPD (kPa). (C) Average wind speed (km/h) ± SD. (D) Cumulative solar radiation (kW/m2). (E) Cumulative UV dose (mJ/cm2). (F) Total emersion time (hrs). ........................................................................ 46 Figure 3.3. Balanus glandula. A) Number of daily cyprid settlers per quadrat (average ± SD). B) Total cyprid cohort mortality (%)...................................................................... 47 viii Figure 3.4. Survivorship of juvenile Balanus glandula up to 10 d post-metamorphosis on bare surfaces and under Fucus spp. cover. ................................................................. 48 Figure 3.5. Cyprid cohort mortality (arcsine transformed data) as a function of principal component factor 3, which is negatively associated with wind speed and wave height. Solid line represents the linear regression. ..................................................................... 50 Figure 3.6. Comparison of surfaces with and without the cover of Fucus spp. A) Number of Balanus glandula cyprid settlers in each daily cohort (average ± SE). B) Total mortality of B. glandula cyprids in each daily cohort. .................................................... 52 Figure 3.7. Proportion of dead Balanus glandula cyprids that were dislodged in the first 2 d after settlement and of those that remained attached to the substratum up to day 3 after settlement, in each of the 2 treatments. . ........................................................................ 53 Figure 3.8. Comparison of (A) average temperature (°C) ± SE and (B) average VPD (kPa) ± SE between rock surfaces with and without the presence of Fucus spp. during the final hour of low tide on 6 of the settlement days. .......................................................... 54 Figure A.1. Results of autocorrelation analysis of residuals from multiple regression models predicting intertidal temperature (A&B) and intertidal relative humidity (C&D). .......................................................................................................................... 72 Figure B.1. Temperature (°C), relative humidity (%), and vapour pressure deficit (kPa) data collected at 3 intertidal heights at Grappler Inlet. .................................................... 74 ix LIST OF TABLES Table 2.1. Multiple regression best-fit model predicting intertidal RH from weather station parameters in 2011.. ........................................................................................... 17 Table 2.2. Two-factor ANOVA of the average mortality of mussels in each of 4 size classes exposed to various VPD levels for 6 h. ............................................................... 26 Table 3.1. Multiple regression best-fit model that predicts intertidal temperature from weather station parameters.. ........................................................................................... 43 Table 3.2. Results of principal components analysis of weather parameters on bare and algae plots at Wizard Islet. ............................................................................................. 49 Table 3.3. Multiple regression best-fit model analyzing the influence of PCA factors on cyprid cohort mortality. ................................................................................................. 49 Table 3.4. Random complete block ANOVA of (A) settlement and (B) mortality in each daily cohort on bare surfaces and under Fucus spp. cover, with the day of the survey as the blocking factor. ........................................................................................................ 51 Table 3.5. Randomized complete block ANOVA of (A) temperature and (B) VPD on bare surfaces and under Fucus spp. cover, with the date as the blocking factor............... 54 1 CHAPTER 1: General Introduction Populations of marine intertidal invertebrates, such as mussels, barnacles, seastars, and crabs, vary in abundance over time (year to year) and space (from one location to another). In many species these variations can be substantial, differing by several orders of magnitude (Berger et al., 2006; Bao et al., 2007; Broitman et al., 2008; Pedersen et al., 2008). Several potential causes of these variations have been investigated, and for many benthic invertebrates the number of individuals colonizing intertidal habitats is affected by larval supply (Grosberg, 1982; Gaines et al., 1985; Minchinton & Scheibling, 1991) and settlement cues (Raimondi, 1988; Pawlik, 1992; Holmes et al., 2005; Jenkins, 2005). However, there is debate over whether these are the predominant influences of population abundance, or if factors affecting post-settlement survival are the most important indicators of abundance (Lively et al., 1993; Gosselin & Chia, 1995; Hunt & Scheibling 1997; Jarrett, 2000; Petraitis et al., 2003; Gosselin & Jones, 2010). Settlement and metamorphosis occur in many invertebrate species with pelagic larvae, and these processes constitute a dramatic ecological transition into new habitat to which settlers must quickly adapt to survive (Werner & Gilliam, 1984); in most cases, individuals will experience air exposure within a few hours of settlement. Most cohorts experience 60 – 99% mortality in the first few days and weeks of life after settlement, (Gosselin & Qian, 1997; Pedersen et al., 2008), therefore it has been suggested that variations in survival through the first few days of life in this new habitat may be the reason for observed differences in population abundance (Osman et al., 1992; Gosselin & Chia, 1995). Variation in post-settlement survival may be influenced by both biological and environmental factors. Biological factors, including predation (Hurlbut, 1991; Lively et al., 1993), dislodgement (Dayton, 1971; Chan & Williams, 2003), and competition (Young & Chia, 1984; Dungan, 1985), are often documented as the cause of early post- settlement mortality. However, it has been suggested that environmental factors that fluctuate to extremes over a short period might be more important causes of mortality (Gosselin & Qian, 1997), which may include temperature stress (Gosselin & Chia, 1995; Chan & Williams, 2003), desiccation stress (Denley & Underwood, 1979; Shanks, 2009),