Not all space is created equal: distribution of free space and its influence on heat-stress and the limpet Patelloida latistrigata

For most marine benthic communities unoccupied primary substrata, or free space, is considered the principle limiting resource. Substratum temperatures, desiccation rates and hydrodynamic characteristics of free space, however, may vary depending on patch size and isolation and therefore potentially influence biotic processes. This paper investigates the relationship between small-scale changes in the availability and configuration of free space, heat stress and abundance of the small rocky intertidal gastropod Patelloida latistrigata within southeastern Australia. Using infrared thermography I show that heat stress of rocky intertidal communities increased linearly with increasing amounts of free space on three neighbouring shores during four separate sampling intervals from October 2009 to January 2010. Abundances of P. latistrigata generally declined with increasing availability of free space and the associated increases in heat stress. An experimental manipulation that altered the configuration but not the availability of free space demonstrated that both heat stress and P. latistrigata abundance are not affected by small-scale changes in the configuration of free space. The small-scale distribution of P. latistrigata, however, was significantly influenced by differences in the configuration of free space with limpets displaying bimodal distributions within areas characterised by unevenly distributed free space. Since the distribution of Patelloida varies depending on the configuration of free space but thermal properties at the scale of individual limpets do not then we might expect Patelloida to be responding to changes in other abiotic factors, such as hydrodynamic forces and desiccation rates, which may change with the configuration of free space. This study highlights the dynamic and usually unexamined relationship between abiotic stress and the availability and acquisition of resources by marine benthic invertebrates

The effects of temperature on the early life history of the rocky intertidal barnacle Tesseropora rosea

The rocky intertidal zone represents the interface between the marine and terrestrial environment and is considered one of the most thermally complex ecosystems on earth. Biologists have long understood that life within the intertidal zone is considerably influenced by a steep thermal gradient produced by the rising and falling tide. In recent years, however, studies have discovered that numerous small-scale processes, other than elevation in tidal height, can produce mosaic patterns of thermal stress along rocky intertidal shores. Linking this local temperature variability to the physiological and demographic patterns of intertidal invertebrates is an essential first step to understanding how climate change might be expected to influence these communities. The early life history stages of many rocky intertidal invertebrates are particularly vulnerable to heat and desiccation stress and play a key role in structuring adult populations. Therefore, temperature variability may considerably influence important demographic processes within intertidal populations. Nevertheless, temperature measurements are often taken at large spatial scales (10 to 1000m2) while early life history processes are typically measured at much smaller scales, such as at the quadrat-level (10 to 100cm2). Processes that operate at these different spatial scales may produce different patterns of temperature variability and consequently limit our ability to relate an organism’s physiological response to its environment and ultimately the demography of the population. Differences between body temperatures of sessile rocky intertidal invertebrates distributed across local spatial scales (100m) may be substantially influenced by the density and species composition of the surrounding biotic community. By contrast, differences between body temperatures of sessile rocky intertidal invertebrates distributed across large spatial scales (100 to 1000km) most likely reflect geographical variation in temperature. Yet, the characteristics of biotic communities have been shown to vary across both regional and large spatial scales. Thus, local-scale differences in the biotic community may counteract or negate temperature variability caused by larger-scale processes. Such might be the case along the south east coast of Australia where densities of dominant space occupiers vary with latitude. My thesis aimed to examine how large- and small-scale temperature variability influences the early life history processes of the habitat forming rocky intertidal barnacle Tesseropora rosea and to characterise the thermal environment at a range of scales. For the large-scale aspect of this study I investigated whether early life history processes could explain the decline in adult abundances along a latitudinal temperature gradient. I then assessed the common use of satellites and terrestrial weather stations as proxies of in situ rocky intertidal water and air temperatures, respectively. This was in order to determine the most appropriate method for measuring rocky intertidal temperature variability. Due to the high variability detected by loggers within a single shore, I next used infrared (IR) imagery to characterise fine-scale temperature variability relevant to recently settled larvae. By undertaking a series of manipulative experiments I investigated how this fine-scale temperature variability influences the settlement and early post-settlement growth and survival of T. rosea. The large-scale component of this study initially revealed that abundances of adult T. rosea decline with increasing latitude, suggesting that important demographic processes, such as settlement and early mortality (i.e. recruitment), may be particularly vulnerable to changes in sea surface temperatures. However, sampling across 11 rocky shores spanning 450km over a two year period did not reveal any latitudinal gradients in either the production, settlement or early post-settlement mortality of larvae even though in situ temperature measurements confirmed the existence of a latitudinal temperature gradient. Indeed, settlement and adult mortality were highly variable among locations and the original decline in adult abundance observed during February 2007 was no longer present in December 2008. These results indicate that local variation in early life-history processes and adult mortality dictate regional variability and observed latitudinal patterns of adult T. rosea abundance. Such local variation in early life-history processes and adult mortality may reflect high temperature variability at these localscales. Therefore, local temperature variability may be an important factor governing biogeographic patterns of abundance. Large-scale settlement and recruitment studies commonly use remote sensing to characterise the thermal environment of recently settled larvae. The use of these temperature measurements have yet to be validated as useful surrogates of in situ temperature variability. Although I found that daily and monthly average temperatures derived from satellites and terrestrial weather stations were significantly correlated, the temperatures reported were considerably different from temperatures derived from in situ data loggers. Daily satellite sea surface temperatures (SSTs) were up to 6.7°C, and on average 1°C, higher than in situ water temperatures, while daily maximum air temperatures measured by weather stations were up to 23.2°C, and on average 4.2°C, lower than in situ air temperatures over a 14-month period. The frequency, duration and number of days greater than 30°C, as well as rates of temperature change, were all significantly lower when measured by weather stations. These differences suggest that satellite SSTs and weather stations are ineffective at capturing extremes in intertidal water and air temperature variability, which considerably influence biological processes. Therefore, to understand the impacts of temperature variability on populations at scales relevant to demographic processes we need to use emerging data logger and infrared technology. Despite the fact that experimental manipulations are essential for determining causation, there are few studies that successfully manipulate temperatures on rocky intertidal shores to test for effects on early life history processes. I used different coloured settlement plates deployed within the mid shore region to experimentally alter the substratum temperatures experienced by newly settled T. rosea larvae. I found that maximum mean surface temperatures of black and grey plates were 5.8°C and 4.8°C warmer than white plates, respectively. Black and grey plates over the entire sampling period were on average 2.2°C and 1.6°C warmer than white plates, respectively. Importantly, cooler white plates had significantly greater settlement and early postsettlement growth of T. rosea than warmer black plates. However, temperature differences between black and white plates did not influence early survival and recruitment. Substratum temperatures of unmodified areas within mid intertidal regions increased with increasing free space (r2=0.75, pT. rosea. Therefore, I undertook a manipulative thermal experiment that altered mid intertidal rock temperatures (which considerably influence body temperatures of recently settled T. rosea) by manipulating the amount of free space, a limiting resource for benthic invertebrates. Quadrats withT. rosea. Here, I found that natural temperature variability between quadrats with 100% free space (i.e. across areas that were unmanipulated) significantly influenced the early post-settlement growth and survival of T. rosea. Such among-quadrat variation at the same tidal height on shore is both underappreciated and a potentially confounding factor in studies of recruitment and population dynamics. Finally, I used IR imagery to test the hypothesis that in situ rocky substrates exhibit repeatable ultra fine-scale (1mm) temperature variation during aerial exposure and that this variability significantly influences early life history processes of T. rosea. Here, larval settlement did not vary with ultra fine-scale variation in rock temperature, but early post-settlement growth and survival were both inversely related to temperature variability at this scale. Furthermore, I found that rock temperatures decreased significantly with increasing proximity to adult T. rosea and that larvae that settled within 15mm of adults survived better than those that settled within 16-30mm. This is partially explained by conspecific adults shading rock and reducing rock temperatures. These results demonstrate, for the first time, that fine-scale variation in thermal stress impacts the early-life history stages of a benthic marine invertebrate. The results of my research have broad ranging implications for understanding how rocky intertidal invertebrates will respond to increasing temperatures and extreme events associated with climate change. Firstly, the geographic distribution of T. rosea does not appear to be limited by a reduction in air and seawater temperatures towards its southern range limit and therefore increasing temperatures may not cause T. rosea to extend its southern distribution. Secondly, broad-scale temperature measurements derived from weather stations and satellites are not the most appropriate estimates of rocky intertidal temperature variability. Therefore, climate change models and predictions should preferentially use local-scale, or better yet, estimates of temperature variability relevant to individuals. Thirdly, the thermal manipulations developed in this study may be particularly useful for simulating the effects of future temperature variability or extreme temperature events on intertidal communities because they can directly elevate body temperatures to reflect future scenarios and do not require longterm monitoring or extreme weather to simulate extreme events. Finally, the high within site temperature variability revealed by IR imaging may override the effect of largescale temperature variability on intertidal populations and reduce our ability to predict the effects of climate change on species distributions. In summary, numerous factors need to be considered when assessing the effect of temperature on the early life history processes of intertidal invertebrates, including consistent small-scale temperature variability. The results of this study show that for a single species, the effects of temperature not only vary during different life history stages, but also, across different spatial scales. These findings contribute to, and advance, the growing body of work that highlights the importance of small-scale temperature variability in influencing the biogeographic and physiological responses of rocky intertidal communities in the face of climate change

Infrared thermography in marine ecology: methods, previous applications and future challenges

Infrared thermography (IRT) is being increasingly utilised by animal physiologists and ecologists to investigate the role of thermal stress and small-scale thermal variability on the distribution and abundance of species. Due to the inability of infrared cameras to work underwater, ecological studies that use IRT have largely been undertaken on terrestrial systems, while fundamentally limited to surfacing mammals in aquatic ecosystems. In recent years, however, IRT has been used to investigate the thermal ecology of intertidal organisms, which are intermittently exposed. The aim of this paper was to summarise the rapidly growing application of IRT in marine ecology, to discuss best practises for using IRT in the marine environment whilst outlining some common limitations, and to suggest future research directions. IRT has been successfully used to count and track the movements of a range of marine mammals as well as to quantify previously unobserved nocturnal feeding patterns. On rocky intertidal shores, IRT has largely been used to assess thermoregulatory processes in gastropods, mussels and sea stars and the effect of heat stress on barnacle recruitment. Ground-truthing and calibration procedures still remain the largest drawback for the use of IRT in ecological studies. However, once the appropriate calculations and working procedures have been implemented, thermal imaging is a reliable and rapid tool for measuring environmental and biological temperature variability. We believe such techniques will become increasingly popular as global temperatures, and hence thermal stress, continue to rise

Rocky intertidal temperature variability along the southeast coast of Australia: comparing data from in situ loggers, satellite-derived SST and terrestrial weather stations

Predicting how both spatial and temporal variation in sea and air temperature influence the distribution of intertidal organisms is a pressing issue. We used data from satellites, weather stations and in situ loggers to test the hypothesis that satellite-derived sea surface temperatures (SSTs) and weather station air temperatures provide accurate estimates of ambient temperature variability on rocky intertidal shores for temporal (hourly for 1 yr) and spatial (10 m to 400 km) variation along the southeast coast of Australia. We also tested whether satellites and weather stations accurately detect the duration, frequency and number of extreme temperature events. Daily mean satellite SSTs and weather station air temperatures were significantly and strongly correlated with intertidal water and air temperatures, respectively (water: r2 = 0.62, air: r2 = 0.63). Nevertheless, depending on location, daily satellite SSTs were up to 6.7°C, and on average 1°C, higher than in situ water temperatures, while daily maximum air temperatures measured by weather stations were up to 23.2°C, and on average 4.2°C, lower than in situ air temperatures. At all locations, the frequency, duration and number of days greater than 30°C, as well as rates of temperature change, were all significantly lower when measured by weather stations. These differences suggest that satellite SSTs and weather stations are ineffective at capturing extremes in intertidal water and air temperature variability. We reinforce the argument that in situ measurements that focus on biologically relevant variation are the only legitimate means of predicting the effects of temperature change on intertidal taxa. © Inter-Research 2011

Estimating latitudinal variability in extreme heat stress on rocky intertidal shores

Aim Broad-scale patterns of heat stress play an important role in shaping the geographical distributions of many species and may differ from large-scale changes in average temperatures. For species living on rocky intertidal shores extreme heat stress occurs when hot dry aerial conditions coincide with midday low tides. We used empirical and modelled temperature data, and estimates of cumulative aerial exposure and solar radiation, in order to test the hypothesis that heat stress on Australian rocky intertidal shores decreases with increasing latitude. Location Rocky intertidal shores of south-eastern Australia spanning \u3e 1500 km and 13° of latitude (26°24′23″ S to 39°07′47″ S). Methods In situ temperature measurements, hourly tidal elevations and daily solar radiation taken over three consecutive summers (December 2009-February 2012) were used to quantify latitudinal variability in extreme heat stress, cumulative aerial exposure and solar radiation, respectively. Comparisons between hourly in situ temperatures and meteorological data were used to produce a large-scale statistical model capable of estimating intertidal substratum temperatures during daytime low-tides, which was then extrapolated across 22 locations. Results Heat stress estimated using in situ loggers deployed across five east coast locations typically did not decline with increasing latitude and neither did midday exposure or solar radiation. The meteorological model proved to be a successful method for estimating rocky shore heat stress and in contrast to the empirical data displayed strong latitudinal trends in mean daily maxima and cumulative heat stress. Modelled acute heat stress (i.e. summer maxima), however, did not decline with increasing latitude, as there was greater thermal variability at higher latitudes. Main conclusions The meteorological model developed in this study represents a useful approach for estimating broad-scale patterns of heat stress on rocky intertidal shores. Results also indicate that latitudinal patterns of acute and chronic heat stress may differ from average temperatures, which are commonly assumed to decline with increasing latitude. Such broad-scale patterns of thermal stress as described in this study will significantly contribute to our ability to understand the impact of climate change on vulnerable rocky intertidal communities

Impacts of Cattle on the Vegetation Structure of Mangroves

Across the globe coastal wetlands have been lost and degraded due to agriculture. Here we test hypotheses that there are differences in vegetation structure of the mangrove Avicennia marina at locations with or without cattle in the lower Shoalhaven River Estuary in New South Wales, Australia. We sampled the pneumatophores, seedlings, saplings, and trees within the mangrove forest and landward of the forest where cattle are most active. Areas with cattle had fewer trees, and their lowest branches were more than 2 m above the ground, giving trees an umbrella-shaped morphology. Although abundances of saplings and seedlings were highly variable among locations, plants at both stages were shortest along the landward side of the forest in the presence of cattle and seedlings were bushier, suggesting consumption of the apical shoots. A reduction in pneumatophore density and the highest proportion of branched pneumatophores occurred along the landward side of the forest in the presence of cattle, indicating impacts of trampling. Prospects for regeneration of the mangroves in the presence of cattle appear limited due to grazing, physical disturbance and trampling across multiple life history stages. Livestock paddocks should be fenced to exclude cattle and prevent degradation of these coastal intertidal habitats

Facing the heat: does desiccation and thermal stress explain patterns of orientation in an intertidal invertebrate?

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. A key challenge for ecologists is to quantify, explain and predict the ecology and behaviour of animals from knowledge of their basic physiology. Compared to our knowledge of many other types of distribution and behaviour, and how these are linked to individual function, we have a poor level of understanding of the causal basis for orientation behaviours. Most explanations for patterns of animal orientation assume that animals will modify their exposure to environmental factors by altering their orientation. We used a keystone grazer on rocky shores, the limpet Cellana tramoserica, to test this idea. Manipulative experiments were done to evaluate whether orientation during emersion affected limpet desiccation or body temperature. Body temperature was determined from infrared thermography, a technique that minimises disturbance to the test organism. No causal relationships were found between orientation and (i) level of desiccation and (ii) their body temperature. These results add to the growing knowledge that responses to desiccation and thermal stress may be less important in modifying the behaviour of intertidal organisms than previously supposed and that thermoregulation does not always reflect patterns of animal orientation.Much of what we understand about orientation comes from studies of animals able to modify orientation over very short time scales. Our data suggests that for animals whose location is less flexible, orientation decisions may have less to do with responses to environmental factors and more to do with structural habitat properties or intrinsic individual attributes. Therefore we suggest future studies into processes affecting orientation must include organisms with differing levels of behavioural plasticity

Using infrared imagery to test for quadrat-level temperature variation and effects on the early life history of a rocky-shore barnacle

Most rocky intertidal studies examine early life-history processes at the quadrat level, but few, if any, have measured temperature variation at this scale in the field. This is surprising because the early life stages of rockyshore invertebrates are considered particularly vulnerable to thermal and desiccation stresses and recruitment processes play a key role in structuring adult populations. We used infrared imagery to quantify in situ variation in rock temperatures during aerial exposure among 35 to 50 400-cm2 quadrats (a typical size utilized in intertidal studies). We test whether natural variation in or experimental manipulation of free space, a potential limiting resource, influences temperature variability among quadrats. We then ask whether quadrat-scale temperature variability and the availability of free space influence the early life-history processes of the habitat-forming barnacle Tesseropora rosea in southeastern Australia. Rock temperatures within quadrats separated by tens of meters differed by up to 8.2uC and temperatures within both natural and manipulated quadrats were positively related to free space. Early postsettlement performance was significantly related to this quadrat-scale temperature variability. In unmanipulated quadrats with 100% free space, settlers in consistently ‘‘warmer’’ quadrats displayed reduced early growth and survival compared with settlers in consistently ‘‘cooler’’ quadrats (growth: r2 5 0.48, p 5 0.001, n 5 18; survival: r2 5 0.41, p , 0.01, n 5 17). Although rock temperatures varied significantly with free space, early postsettlement growth and survival did not. Our results highlight both the strong response of early life stages to large natural variation in rock temperatures and the consequent importance of considering quadrat-scale temperature variation in future manipulative experiments

Biogeographical patterns of rocky shore community structure in south-east Australia: effects of oceanographic conditions and heat stress

Aim Environmental variability can be a major driver of large-scale patterns of distribution and abundance and, within the marine environment, benthic community structure is usually thought to reflect several oceanographic processes and coastal morphological features. The aim of this study was to quantify spatial and temporal variability in large-scale rocky intertidal community structure along the south-east coast of Australia and ask whether these are associated with variation in sea-surface temperatures, chlorophyll-a concentration, heat stress and coastal geomorphology. Location Rocky intertidal shores of south-east Australia spanning \u3e 1750 km, 13° of latitude (26°24′23″ S to 39°07′47″ S) and known biogeographical barriers. Methods From 2009 to 2011 one-thousand and twenty photoquadrats located within the midshore region of 17 rocky shores (20 quadrats site−1 year−1) were used to estimate spatial and temporal variability in the percentage cover of dominant benthic invertebrates and macroalgae. We used satellite data to generate annual estimates of nearshore sea-surface temperatures (SST) and chlorophyll-a concentrations ([Chl-a]) and a meteorological model to estimate heat stress during summer low-tides. Results Non-metric multidimensional scaling and cluster analysis revealed a strong and consistent biogeographical break in rocky intertidal community structure between southern and eastern sites. Nearshore oceanographic conditions and summer heat stress did not appear to influence this discontinuity as abundances of functional groups (filter-feeders, grazers and macroalgae) generally did not vary in response to geographical patterns of SST, [Chl-a] or mean daily maximum air temperatures during low-tide. At the species level, however, the distribution and abundance of several species varied with nearshore SST and [Chl-a] including the barnacle Tesseropora rosea and limpets within the genus Patelloida, respectively. Main conclusions We found no evidence of strong bottom-up effects on rocky intertidal functional group abundance. This was somewhat expected because bottom-up effects in regions characterized by persistent downwelling are generally weak or non-existent. Instead, broad-scale patterns of community composition were best explained by coastal geomorphology. This study provides an important and necessary comparison for the role of broad-scale environmental variability in structuring marine benthic communities within downwelling rather the more commonly reported upwelling systems

Altering species interactions outweighs the effects of experimental warming in structuring a rocky shore community

The strength and direction of interspecific interactions governing communities is expected to change with increasing global temperatures. However, in many ecosystems it remains unclear which species interactions are most likely to be altered under increasing thermal stress and what impacts, if any, such altered interactions will have on community structure. We investigated the interactive effects of increased temperature and altered species interactions on the structure of a rocky intertidal community by deploying black and white plates in areas with or without the dominant grazer, the limpet Cellana tramoserica. Plates effectively manipulated substratum temperature, whilst anti-fouling paint effectively manipulated the strength of algal-herbivore interactions. Plates without C. tramoserica quickly developed and maintained abundant macroalgal assemblages irrespective of thermal stress. By contrast, the abundance of barnacles remained relatively low and did not differ across thermal treatments, although they were slightly more abundant in plots where C. tramoserica had been excluded. These results support recent findings that altered species interactions are anticipated to have greater effects on community structure than the direct impacts of warming, challenging the view community structure under warming climatic conditions can be predicted from individual responses of populations to increasing thermal stress. Based on these and other recent findings we therefore advocate for greater inclusion of biotic interactions into climate change models that aim to predict the state of future ecological communities