over long time scales, because commercially available temperature loggers were sufficiently small and robust to be deployed for long periods of time. As wtih the organism being monitored, the colour, morphology and mass of a temperature logger can significantly affect the temperature that it records. Therefore, biomimetic sensors/loggers (robomussels) that are specifically matched (modified) to the thermal characteristics of the mussels being measured have been developed. These can provide realistic measurements of body temperature in the field, over a broad variety of temporal and spatial scales (Fitzhenry et al. 2004). Robomussels have the shape, size and colour of actual mussels (Figure 3.4), with miniature built‐in sensors that track temperature inside the mussel beds. The fact that they are self‐contained, robust and inconspicuous makes it unlikely that they will be intentionally destroyed. Robomussels are made from a polyester resin with a black colouring, which is poured into moulds created from Mytilus shells. A TidbiT logger (Figure 3.4) is embedded in the polyester resin, which after hardening is smoothed and shaped to resemble a real mussel. The logger battery lasts for more than five years and the memory stores ~42 000 12‐bit temperature measurements (enough for more than two and a half years) with a sampling frequency of 30 min (can be set from 1 s to 18 hr). The loggers have an accuracy of ±0.20 °C at 0–50 °C (details in Fitzhenry et al. 2004; Lima et al. 2011). In the field, robomussels are usually deployed on hard rock in intact mussel beds using epoxy putty, taking care to ensure that they are completely surrounded by other mussels, since loggers deployed as solitary individuals tend to yield abnormally high readings. Logger programming and data retrieval is done through the instrument’s LEDs, which are exposed on the outside of the robomussel. An optical USB interface allows users to offload data in seconds. Biomimetic loggers have also been used in animals such as limpets, barnacles, snails and seastars. See Helmuth (2002) and Fitzhenry et al. (2004) for the potential pitfalls of logger use, Lima et al. (2011) for different types of biomimetic data loggers and Judge et al. (2018) for recent advances in temperature logging in intertidal systems.
Figure 3.4 A‘robomussel’ (right) molded from polyester resin and containing a TidbiT logger thermally matched to the characteristics of a living mussel. On the left is an unmodified Onset TidbiT logger.
Source: From Fitzhenry et al. (2004). Reproduced with permission from Springer Nature.
In the first study in which robomussels were deployed, Helmuth & Hofmann (2001) continuously monitored temperatures at a location in central California for a period of two years, using loggers designed to mimic the thermal characteristics of M. californianus. Model mussel temperatures were recorded on both a horizontal (Figure 3.5) and a vertical, north‐facing microsite and in an adjacent tidepool. Mussels at each microsite were periodically measured for levels of heat shock proteins (Hsp 70), a measure of thermal stress (Fields et al. 2012). The role of Hsps in the stress response is to assist misfolded proteins to attain or regain their native state and prevent heat‐damaged protein accumulation in cells, thereby preventing the formation of cytotoxic aggregates. Other factors that have a bearing on an individual’s response to thermal stress include: size, shape, mass and colour (Helmuth 2002), vertical position in the sediment (Jost & Helmuth 2007), geographic location (Fields et al. 2012), timing of low tide (Mislan et al. 2009) and interaction with stressors such as anoxia (Veldhuizen‐Tsoerkan et al. 1991), salinity fluctuations (Podlipaeva & Berger 2012), hypoxic conditions (Anestis et al. 2010), reduced food supply (Schneider et al. 2010), pollutants (Mahmood et al. 2014; Banni et al. 2017) and pathogens (Cellura et al. 2007). In Helmuth & Hofmann (2001), mussel temperatures were consistently higher on the horizontal surface than on the vertical one, and differences between these surfaces were reflected in the amount of Hsp70 produced. Temperatures recorded in the tidepool were not as high as those on the exposed horizontal microsite but in general exceeded those recorded on the aerially exposed vertical face. One interesting finding of the study was that seasonal peaks in extreme (acute) high temperatures did not always coincide with peaks in average daily maxima (chronic high temperatures). A subsequent study showed that thermal stress may depend not only on exposure to temperature extremes but also on the thermal history of the temperature signal (Helmuth 2002). For example, on days when daily maximum temperatures increase gradually, mussels may be able to acclimate better to temperature extremes compared to days when temperature maxima are preceded by cool days. Helmuth (2002) also found through deployment of loggers at multiple sites that each site had a unique thermal signature due to interactions of terrestrial climate, tidal cycle and wave exposure, but also significant within‐site differences due to tidal height and substratum angle.
Figure 3.5 Example of fluctuations in temperature experienced over one month (August 1999) at a horizontal microsite. Daily maxima were calculated from temperature data collected every 5–10 min. The highest daily maximum was recorded as the monthly extreme (‘acute’) high temperature at each site. The average of the daily maxima was calculated as a measure of ‘chronic’ high‐temperature exposure. Similarly, average daily minima and monthly minima were calculated.
Source: From Helmuth & Hofmann (2001). Reprinted with permission from The University of Chicago Press.
In a more recent study, Olabarria et al. (2016) investigated the effect of a heatwave on the physiological and behavioural responses in monospecific or mixed aggregations of the invasive mussel Xenostrobus securis, which has successfully colonised the inner part of the Galician Rias Baixas (NW Spain), where it co‐occurs with the commercially important mussel M. galloprovincialis (see Chapter 10). In a mesocosm experiment, mussels were exposed to simulated tidal cycles and similar temperature conditions to those experienced in the field during a heatwave that occurred in the summer of 2013, when field robomussels registered temperatures up to 44.5 °C at low tide. In monospecific aggregations, M. galloprovincialis was more vulnerable than X. securis to heat exposure during emersion. However, in mixed aggregations, the presence of the invader was associated with lower mortality in M. galloprovincialis. The greater sensitivity of M. galloprovincialis to heat exposure was reflected in a higher mortality level, greater induction of Hsp70 protein and higher rates of respiration and gaping activity (opening of shell valves to permit evaporative cooling), which were accompanied by a lower heart rate (bradycardia). It appears that the invader enhanced the physiological performance of M. galloprovincialis, highlighting the importance of species interactions in regulating responses to environmental stress. In a complementary study, Nicastro et al. (2012) found that under conditions of heat stress, aggregations of the gaping mussel P. perna exhibited lower mortality rates than isolated occurences or aggregations of the nongaping mussel M. galloprovincialis, because the gaping behaviour of P. perna ameliorated stressful environmental conditions of mussels through evaporative cooling (see Chapter 7 for details on gaping). The drawback of this response is an increased risk of desiccation. Large mussels have greater amounts of water available in their tissues than small ones (Kennedy 1976; Helmuth 1998), which provides greater protection from desiccation
