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Tidal Dynamics, Topographic Orientation, and Temperature-Mediated Mass Mortalities on Rocky Shores

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Tidal Dynamics, Topographic Orientation, and Temperature-Mediated Mass Mortalities on Rocky Shores Vol. 371: 37–46, 2008 MARINE ECOLOGY PROGRESS SERIES Published November 19 doi: 10.3354/meps07711 Mar Ecol Prog Ser Tidal dynamics, topographic orientation, and temperature-mediated mass mortalities on rocky shores Christopher D. G. Harley* Bodega Marine Laboratory, PO Box 247, Bodega Bay, California 94923, USA Present address: University of British Columbia, Department of Zoology, 6270 University Blvd., Vancouver, British Columbia V6T1Z4, Canada ABSTRACT: Temperature is among the main structuring agents on rocky intertidal shores. Although infrequent mortality events associated with high temperatures have been observed in several inter- tidal taxa, careful documentation of these events is rare, and small-scale variability in mortality patterns remains poorly understood. In Bodega Bay, California, USA, 2 mortality events occurred on exposed rocky shores during the spring of 2004 when low tides occurred around mid-day. Limpets Lottia scabra were killed during unseasonably warm weather in mid-March. In late April, record- high temperatures resulted in widespread mortality of the mussel Mytilus californianus. Levels of mortality for both species were closely associated with small-scale variability in temperature, which in turn was closely associated with substratum orientation. Invertebrates occupying surfaces facing the sun when stress was most intense were much more likely to die than those living on surfaces angled ≥45° away. Because the within-day timing of thermal stress varied seasonally, the highest mortalities were recorded on southwest-facing surfaces on the March afternoon low tide and on southeast-facing surfaces on the April morning low tide. Limpets and mussels showed little mortality during the events that were harmful to the other taxon, suggesting that these different taxa respond to different aspects of their thermal environment. If climate change results in more frequent and more severe episodes of thermal stress, future ecological change may also be heavily dependent on tidal dynamics and small-scale variation in substrate orientation. KEY WORDS: Temperature · Thermal stress · Mass mortality · Substratum orientation · Rocky intertidal zone · Lottia scabra · Mytilus californianus Resale or republication not permitted without written consent of the publisher INTRODUCTION 1984, Leonard 2000, Harley 2003). Daily and seasonal thermal variation drive vertical migration patterns in Temperature is one of the most important environ- the intertidal zone (Janssen 1960, Williams & Morritt mental controls on organismal physiology, perfor- 1995). Longer-term patterns associated with climate mance, and fitness (Hochachka & Somero 2002). The change also drive shifts in the distribution and abun- ecological importance of temperature is particularly dance of intertidal organisms (Barry et al. 1995, South- apparent on rocky intertidal shores, which are among ward et al. 2005). the most thermally variable and stressful habitats on Despite intertidal ecologists’ general acceptance of earth. On rocky shores, temperature drives physiolog- the overarching importance of temperature, docu- ical acclimation and evolutionary adaptation (Schmidt mented mortality following natural periods of intertidal & Rand 1999, Tomanek & Somero 1999, Somero 2002) heat stress is surprisingly rare. In the tropics, heat kills and plays a key role in determining species distribu- have been observed in limpets (Williams et al. 2005), tions (Newell 1979) and community structure (Wethey mussels (Liu & Morton 1994), and barnacles (Liu & *Email: [email protected] © Inter-Research 2008 · www.int-res.com 38 Mar Ecol Prog Ser 371: 37–46, 2008 Morton 1994, Chan et al. 2006). In the temperate zone, ity event occurred in March 2004 and killed a number the few examples of temperature-driven mass of limpets Lottia scabra but did not result in observed mortality events also include limpets (Lewis 1954, mortality in mussels Mytilus californianus. The second Frank 1965, Sutherland 1970, Kohn 1993), mussels event, which killed large numbers of M. californianus (Suchanek 1978, Tsuchiya 1983, Petes et al. 2007), and but few if any L. scabra, occurred during a record-set- juvenile barnacles (Wethey 1984, E. Sotka pers. ting heat wave in April of the same year. Using in situ comm.). Although documented cases may be rare, thermal data, temporal trends in species abundance, infrequent disturbances such as thermally generated and post-mortality observations, I related the mortal- mass mortality events have a variety of ecologically ity observed in these 2 taxa to small-scale spatial important impacts including significant reductions in variability in their thermal environment, and tie these populations of ecological dominants (Turner & Dale patterns into seasonal thermal and tidal dynamics. I 1998). Furthermore, because climate change is pre- hypothesized that (1) invertebrate body temperature dicted to increase both mean temperatures and the fre- varied with substratum orientation, being highest on quency of extreme high temperature events (IPCC surfaces that faced the sun at low tide, (2) mortality 2007), presently rare temperature-associated mass depended on body temperature and therefore varied mortalities may become more common in the future. It with substratum orientation, and (3) the specific is therefore of interest to understand the spatial and spatial pattern of these relationships depended upon temporal patterns of such mortality events in an effort the timing of low tide. to predict how intertidal communities may be affected by thermal stress now and in the future. The susceptibility of a population to a heat-related MATERIALS AND METHODS mortality event depends upon the spatial and temporal distribution of thermal stress, the relationship between Study system. This research was conducted on the environmental temperature and body temperature, wave-exposed rocky shores of the Bodega Marine and the relationship between body temperature and Reserve in northern California, USA (38.36° N, organismal performance. For example, thermal stress 123.1° W). The intertidal area consists of gently sloping varies greatly from one microhabitat to the next, and to nearly vertical granite benches. The organisms cho- organisms on north-facing surfaces in the Northern sen for study, i.e. the limpet Lottia scabra and the mus- hemisphere remain cooler than their counterparts on sel Mytilus californianus, are abundant and ecologi- horizontal or south-facing surfaces (Helmuth & Hof- cally important species in the high- and mid-intertidal mann 2001, Harley 2003, Denny et al. 2006). The rela- zones, respectively. In the high zone, L. scabra lives tionship between the abiotic environment and body among barnacles (primarily Chthamalus dalli and temperature depends on organismal morphology and Balanus glandula) and several species of macroalgae behavior (e.g. Bell 1995, Helmuth 1998, Denny & (most notably Mastocarpus papillatus and Pelvetiopsis Harley 2006). The impact of high body temperature limitata). Even though the northern limit of L. scabra is depends on an individual’s or species’ ability to upreg- found in northern California (Gilman 2006), the spe- ulate physiological protective mechanisms (Stillman cies is still vulnerable to mass mortalities associated 2003) and upon an individual’s or species’ critical with hot, calm weather in this region (Sutherland maximum temperature (Evans 1948, Southward 1958, 1970). Somero 2002). Furthermore, ‘stress’ as perceived by an The mid-intertidal zone in northern California is organism may have as much to do with departures dominated by the mussel Mytilus californianus. M. from the temperature to which the organism is accli- californianus is a competitive dominant and provides a mated as with the actual temperature reached (e.g. habitat for dozens to hundreds of other species Stillman 2003). This complexity makes it difficult to (Suchanek 1992, Smith et al. 2006a). Although there predict the effects of any given thermal stress event. have been reports of temperature-induced mass mor- On rocky shores, our understanding of the ecological talities in other species in the genus Mytilus (Suchanek consequences of thermal stress is further limited by the 1978, Tsuchiya 1983), documentation of heat death in paucity of concurrent measurements of organismal M. californianus is rare. Indeed, the evidence available responses (e.g. mortality) and high-resolution, biologi- from one cool site (Tatoosh Island, Washington) sug- cally relevant thermal time series. gests that the upper limit of M. californianus may be In this study, I took advantage of 2 natural, temper- more closely associated with emersion time than with ature-related mortality events to explore the impor- temperature per se (Denny & Paine 1998, Harley & tance of temporal patterns and small-scale spatial Helmuth 2003). The importance of temperature as a variation in the thermal environment as well as inter- limiting factor for M. californianus at hotter sites is specific differences in susceptibility. The first mortal- poorly understood. Harley: Temperature-mediated mass mortalities 39 Environmental data collection. Predicted tidal data bed, although the loggers may slightly underestimate for Bodega Bay were generated using XTide software mussel body temperatures at high temperatures (www.flaterco.com/xtide/). Long-term air temperature (Fitzhenry et al. 2004). data were obtained from the Bodega Ocean Observing Quantifying mortality in the field. Limpet densities Node (BOON). Air temperature
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