Temperature and Salinity Effects on Shell Selection by the Hermit Crab Pagurus longicarpus.
Hermit crabs have no natural protection for their soft abdomens (Hazlett and Provenzano, 1965), which leaves them vulnerable to predators (Hazlett. 1981), desiccation (Herreid, 1969), and salinity stress (Pechenik et al., 2001). In order to survive, they have to find some sort of shelter, typically a portable one in the form of an empty gastropod shell (Reese, 1962). When a hermit crab is not occupying a good-quality shell that is of ideal size for the animal's weight (Vance, 1972a; Angel, 2000), it will investigate almost any shell it comes across, looking for a potentially better option (Mc-Clintock, 1985). Occupying a shell that is too small increases the likelihood that a hermit crab will suffer from predation (Vance, 1972b) or desiccation (Taylor, 1981), and occupying a shell that is unnecessarily large means that more energy will be expended in carrying the additional weight (Wilber, 1990; Osorno et al., 1998).
When studying hermit crab behavior, it is necessary to provide shells of appropriate size for each individual in order to minimize shell-searching behavior (McClintock, 1985) and to ensure that in shell choice studies (e.g., Pechenik and Lewis, 2000; de la Haye et al., 2011; Pechenik et al., 2015b) the hermit crabs have an ideal shell to choose as an option. To this end, a number of studies have been conducted to determine the shell sizes preferred by hermit crabs of different sizes and species (e.g., Vance, 1972a; Angel, 2000; Briffa and Elwood, 2007). These experiments were all performed at temperatures and salinities typically seen in the habitats of the hermit crabs being studied.
Our study concerns the behavior of the long-wristed hermit crab, Pagurus longicarpus Say, 1817, which can be found along the Atlantic Coast of Canada and the United States from Nova Scotia to Florida, as well as along the Gulf Coast of the United States (Young, 1978). These hermit crabs can be found both intertidally and subtidally (McDermott, 1999), and at low tide they are sometimes stranded in tide pools (Fraenkel, 1960). Conditions in tide pools can change rapidly, depending on the weather on a given day (Fraenkel, 1960). On hot, sunny days, the temperature and salinity in a tide pool can increase rapidly (Fraenkel, 1960; Koprivnikar and Poulin, 2009), and on rainy days, the salinity can rapidly decrease (Montory et al., 2016). Even more abrupt changes can occur when a rising tide floods into tide pools, returning the temperature and salinity to more average levels (Fraenkel, 1960; Bergerand Kharazova, 1997). As the effects of climate change begin to be felt more strongly (IPCC, 2014), the changes in tide pool physical conditions will likely become more extreme and erratic as well.
Previous studies have examined some of the effects of changing environmental conditions on some aspects of hermit crab physiology and behavior. Changes in temperature have been shown to make the startle response of hermit crabs less predictable (Briffa et al., 2013), and decreases in salinity have been shown to cause hermit crabs to retract into their shells and reduce their rates of oxygen consumption (Davenport et al., 1980). However, we are not aware of any studies that have examined how the sizes of shells chosen by long-wristed hermit crabs (P. longicarpus) are affected by changes in temperature or salinity. In this study, we set out to determine whether shell size preferences for P. longicarpus were affected by changes in temperature or salinity that could be experienced in tide pools currently or in the near future.
Materials and Methods
Periwinkle shell collection and preparation
Most of the hermit crabs (Pagurus longicarpus Say, 1817) at our study site were found living in periwinkle (Littorina littorea) shells (Pechenik and Lewis, 2000; Pechenik et al., 2015a; SCG and JAP, pers. obs.). Live periwinkles with shell aperture lengths ranging between 7.6 and 19.1 mm (mean length = 14.3 mm, median length = 14.4 mm, standard deviation [SD] = 2.4 mm, N = 353 shells) were collected haphazardly from the rocky intertidal zone at Beverly, Massachusetts, in February 2016, and then taken on ice to Tufts University, where they were euthanized by freezing. The dead periwinkles were then placed in room-temperature seawater (a mixture of Instant Ocean [Spectrum, Blacksburg, VA] and 1-[micro]m filtered seawater, ~30 ppt salinity) and allowed to decompose for several weeks. The water was changed periodically until no decomposed tissue was visible in the discarded water. After the tissue decomposition process was complete, the shells were scrubbed with a bristled brush to remove any algal buildup, rinsed several times in tap water, and inspected to ensure that they were free of symbionts such as Crepidula convexa (Li and Pechenik, 2004), Crepidula plana (Pechenik et al., 2015b), Hydractinia spp. (Bach et al., 2006), and barnacles (McDer-mott, 2001).
In order to determine the relationship between shell aperture length and dry shell weight, a haphazardly selected subset of intact shells collected locally within the previous 10 years was measured to the nearest 0.1 mm and weighed to the nearest 0.001 g.
Hermit crab collection and care
Hermit crabs (P. longicarpus) occupying periwinkle shells were collected haphazardly from the rocky intertidal zone at Nahant, Massachusetts, in the late spring of 2016, when the water temperature in the subtidal zone was approximately 22 [degrees]C and the water temperature in tide pools was as high as 27 [degrees]C. The hermit crabs were transported to Tufts University, where they were kept in laboratory aquaria containing continuously aerated artificial seawater (Instant Ocean, called "seawater" from now on) at 30 ppt salinity and room temperature (~22 [degrees]C). The hermit crabs were fed in smaller plastic containers of seawater three times per week (to prevent waste buildup in the larger aquaria) on a diet of artificial crab meat (transOCEAN, Bellingham, WA; Alaskan pollack and king crab) and shrimp pellets (Ocean Star International, Burlin-game, CA). After feeding, they were returned to the aquaria. The hermit crabs were allowed to acclimate to laboratory conditions for one to three weeks before experiments began. No hermit crab was used in more than one trial. After experimentation, the hermit crabs were returned to the collection site.
Evaluating the size of shells chosen at different temperatures and salinities
Experiments were conducted to determine the shell sizes preferred by hermit crabs under potentially stressful conditions, following the general procedures of Angel (2000) and Vance (1972a). Fifty hermit crabs that had both of their che-lipeds intact were used in each experimental treatment. Each of the hermit crabs was free from visible parasites (McDer-mott, 2001), although some were occupying damaged shells or shells with attached symbionts, such as Crepidula spp., barnacles, Hydractinia spp., and coralline red algae, because these were the shells they were collected in (although individuals may have exchanged shells with one another since the date of collection). Hermit crabs were fed on the day before being used in an experiment and were then placed in a new 20-L aquarium filled with continuously aerated seawater under control conditions (22 [degrees]C and 30 ppt salinity), one of two altered temperatures (32 [degrees]C and 30 ppt, simulating possible thermal conditions in a tide pool on a hot day, or 16 [degrees]C and 30 ppt), or one of three altered salinities (22 [degrees]C and 40 ppt, simulating possible salinity conditions in a tide pool on a sunny, hot day; 22 [degrees]C and 20 ppt, simulating possible conditions in a tide pool on a rainy day; or 22 [degrees]C and 15 ppt, simulating the impact of even higher levels of precipitation).
After the 50 hermit crabs had been acclimated for 24 h to the new temperature or salinity conditions (or, in the case of the control animals, 24 h at the unaltered control temperature and salinity levels), 250 intact, empty shells ranging in aperture length from 7.6 to 19.1 mm (selected haphazardly from those collected at Beverly, MA) were added to the aquarium, for a total of 300 shells, including the 50 shells that the hermit crabs started out in. The hermit crabs were then given 48 h to investigate their options, during which time they were not disturbed by the experimenters.
After the 48 h, their final shell choices were recorded (Vance, 1972a; Angel, 2000). The hermit crabs were placed individually in cups with room-temperature, 30 ppt seawater, and individuals were removed from their shells by heating the seawater to about 34 [degrees]C; individuals of the species P. longicarpus recover rapidly following removal when using this procedure (Pechenik et al., 2015b). The hermit crabs were then blotted dry and massed to the nearest milligram, and shell aperture lengths were measured with calipers to the nearest 0.1 mm; shell aperture length is commonly used to represent shell size, because shells in the field frequently have damaged apexes, making it impossible to measure shell length (e.g., Angel, 2000; Pechenik and Lewis, 2000). Any gravid female hermit crabs or hermit crabs found to be missing one or both of their chelipeds at the end of the experiment were discarded from the analysis. The sizes of the hermit crabs in each treatment are detailed in Table 1.
The results were plotted on a log scale, and the lines of best fit for each experimental group were compared to those for every other group by linear regression in Prism, version 7.02 (GraphPad Software, San Diego, CA).
In order to determine whether the shell sizes preferred by long-wristed hermit crabs (P. longicarpus) in the field at Na-hant have remained constant over the years, our results at 16 [degrees]C were compared to those obtained by Angel (2000) at 18 [degrees]C in a similar study roughly 20 years ago. We approximated the preferred shell sizes recorded by Angel based on a figure from her paper (Angel included gravid females in her results), and we compared them to our data at 16 [degrees]C by using a linear regression.
There was a strong relationship between the shell aperture length and dry weight of the empty periwinkle shells that had been collected over the past 10 years (Fig. 1). An increase in shell aperture length from only 12 to 13 mm corresponded to an almost 40% increase in shell dry weight, and an even smaller increase in shell aperture length from 12 to 12.1 mm corresponded to an almost 4% increase in shell dry weight.
When examined after 48 h, larger hermit crabs had chosen to occupy larger shells under all experimental conditions ([r.sup.2] of at least 0.76 for each treatment) (Figs. 2, 3). However, the shell sizes occupied by hermit crabs of a given size were significantly altered under several of the temperature and salinity treatments, when compared to the control treatment. In particular, the slope of the line of best fit (linear regression analysis) for hermit crabs in the control treatment (22 [degrees]C, 30 ppt) was significantly different from the slopes of the lines of best fit for hermit crabs in both the 16 [degrees]C treatment (F = 7.678, P < 0.01) and the 32 [degrees]C treatment (F = 5.849, P = 0.02) (Fig. 2). Reducing the salinity to 15 ppt also significantly affected the sizes of shells chosen (F = 4.485, P = 0.04) (Fig. 3A), although the control slope was not significantly different from that for shells chosen by hermit crabs in either the 20 ppt salinity treatment (F = 1.638, P = 0.21) or the 40 ppt salinity treatment (F = 1.348, P = 0.25) (Fig. 3B, C). The sizes of shells chosen were not significantly different (P > 0.05) when the results of any of the altered temperature or altered salinity treatments were compared to one another.
The original shells that the hermit crabs were occupying at the start of the experiment had not been marked with ink or in any other manner, due to concerns that such imperfections might influence the hermit crabs' shell choice decisions, so there was no way to determine whether all of the hermit crabs switched shells. However, the presence of empty, damaged shells in each of the tanks at the end of the experiment indicated that many hermit crabs had switched shells, because none of the 250 intact, empty shells that they had been provided with had any visible damage.
Linear regressions comparing our data to those collected for the same species by Angel (2000) suggest that the shell size preferences of long-wristed hermit crabs at this study site have not changed appreciably over the past 20 years. The slope of our approximated line of best fit for Angel's 18 [degrees]C data was not significantly different from the slope of the line obtained in our study at 16 [degrees]C(F = 0.197, P = 0.66) (Fig. 4).
As noted in the Introduction, a hermit crab in a shell too small for its mass is more likely to suffer from predation (Vance, 1972b), desiccation (Taylor, 1981), and a decreased growth rate (Angel, 2000) than a hermit crab in a shell of ideal size. Moreover, a hermit crab in a shell that is too large will expend more energy than is necessary to carry a suitably protective shell (Wilber, 1990; Osorno et al., 1998). We observed significant differences in preferred shell size between hermit crabs maintained under control conditions (22 [degrees]C and 30 ppt salinity) and those maintained at both the lower temperature of 16 [degrees]C and the higher temperature of 32 [degrees]C (Fig. 2).
Seven hermit crabs were found to have died at the end of the 32 [degrees]C experiment--more than in any other treatment--suggesting that this high temperature was likely stressful for this population of Pagurus longicarpus. Generally, at both the lowered and elevated temperatures, small hermit crabs preferred shells with slightly smaller aperture lengths than the shells that similarly sized hermit crabs chose under control conditions, while large hermit crabs preferred shells with slightly larger aperture lengths than the shells that similarly sized hermit crabs chose under control conditions.
Reducing the salinity from 30 to 20 ppt did not significantly alter shell size preferences, but reducing the salinity to 15 ppt did (Fig. 3A, B). As with the hermit crabs at 16 [degrees]C and 32 [degrees]C, the smaller hermit crabs preferred slightly smaller shells than hermit crabs of the same size maintained under control conditions, and larger hermit crabs preferred slightly larger shells than those tested under control conditions.
There was no significant difference in the size of shells chosen by hermit crabs maintained under control conditions versus those that had been held at the high salinity of 40 ppt (Fig. 3C). We observed seawater in tide pools at Nahant at low tide reaching a maximum salinity of 38 ppt in the summer of 2016 (whereas the salinity subtidally was around 30 ppt), suggesting that the hermit crabs are already surviving at salinities close to our experimental high salinity of 40 ppt. On the warmer days that are predicted for the future (IPCC, 2014), with higher levels of evaporation, it is reasonable to expect that the salinity in tide pools may sometimes exceed 40 ppt. Future studies thus might consider whether even higher salinity levels might significantly affect the shell size choice of long-wristed hermit crabs.
We would not expect hermit crabs to knowingly choose to occupy shells that might put them in danger. However, the direction of changes in shell size preference that we observed were consistent in all experimental treatments when compared to the shells occupied by the control hermit crabs. Excluding the control treatment, none of our tested treatments produced results that differed significantly from one another. This suggests that the substantial changes in temperature and salinity experienced by our hermit crabs did not render them incapable of distinguishing between shells of different sizes. The response to shifts to potentially stressful environmental conditions might not be specific to the type or direction of the shift. Instead, it might be a more generalized response to fluctuating environmental conditions. This raises the question of why the hermit crabs might be shifting their shell size preference.
As noted earlier, while the differences that we observed in preferred shell sizes were often only a few tenths of a millimeter, the corresponding differences in shell weight were much greater. For instance, our results suggest that a 150-mg hermit crab under control conditions would prefer a shell 1.25 times the weight preferred by a hermit crab of the same size at 16 [degrees]C, 1.71 times the weight preferred by a hermit crab of the same size at 32 [degrees]C, and 1.77 times the weight preferred by a hermit crab of the same size at 15 ppt. A 1-g hermit crab under control conditions would prefer a shell 0.80 times the weight of a shell preferred by a hermit crab at 16 [degrees]C, 0.89 times the weight of a shell preferred by a hermit crab at 32 [degrees]C, and 0.94 times the weight of a shell preferred by a hermit crab at 15 ppt.
Thus, a hermit crab choosing a smaller shell than normal could be making a selection based on shell weight: if higher than usual amounts of energy are being expended to maintain normal functions in response to stressful conditions, a smaller, lighter shell could indicate a desire to conserve as much energy as possible, while still possessing a shelter that provides some protection (Herreid and Full, 1986; Osomo et al., 1998). Alternatively, a hermit crab choosing a larger shell could be seeking out a shelter with greater internal volume, so that it could retract farther than usual, perhaps to better avoid predators that it may not have the energy to fight or flee from (Briffa and El-wood, 2004). Additionally, occupying larger shells can result in faster growth (Fotheringham, 1976; Bertness, 1981a;Black-stone, 1985; Angel, 2000; Alcaraz et at, 2015), and larger shells can hold more water in their interiors, providing a greater buffer against a fluctuating environment (Bertness, 1982). It remains to be determined whether selecting shells of different sizes in response to changes in temperature or salinity affects hermit crabs' vulnerability to predation or dessication or whether it results in an altered growth rate.
But none of this explains why smaller crabs experiencing changes in temperature or salinity preferred smaller than average shells while the larger crabs experiencing the same conditions preferred larger than average shells. This could have been an artifact, because the hermit crabs that were collected haphazardly for the control treatment were, on average, larger than those collected haphazardly for most of the other treatments. It is also possible that the difference is related to sex, because adult male long-wristed hermit crabs reach larger sizes than adult females (Blackstone and Joslyn, 1984). Female hermit crabs occupying shells that are substantially larger than the preferred shell size have been shown to brood eggs less frequently, possibly in order to devote energy to growth (Bertness, 1981b; Hazlett et al., 2005). Perhaps the females do not brood eggs at certain temperatures and salinities and thus would require smaller shells if not devoting energy to growth (Childress, 1972; Bertness, 1981a; Hazlett, 1981).
Long-wristed hermit crabs in the intertidal zone are potentially exposed to temperature and salinity shifts multiple times a day (Fraenkel, 1960; Kopri vnikar and Poulin, 2009; Montory et al., 2016). In habitats such as Nahant, where the supply of high-quality empty shells is often limited (Pechenik et al., 2015a), a frequently shifting pattern of shell preference could lead to an increased amount of time spent actively seeking out and fighting for new shells (Hazlett, 1966; Dowds and El-wood, 1983)--time that could otherwise be spent hunting for food or mates. Future studies could examine whether hermit crabs exposed to periodically oscillating temperatures and salinities--as might be expected to occur routinely in the intertidal zone--or seasonal changes in temperature will exhibit shifts in shell size preferences as often as the conditions change. Additionally, the effects of simultaneous changes in temperature and salinity could be studied to determine whether changes in both lead to any sort of additional effect.
The shell sizes preferred by long-wristed hermit crabs at Nahant have apparently not changed over the past 20 years. The laboratory study designed by Angel (2000) was conducted at 18 [degrees]C, and while we did not conduct a trial at that exact temperature, the results from her study were not significantly different from the results that we obtained at 16 [degrees]C (Fig. 4). Studies such as these should be replicated with individuals from warmer climates, because long-wristed hermit crabs can be found along the southern Atlantic and Gulf Coasts of the United States (Young et al., 2002). It would be interesting to know whether individuals acclimated to warmer temperatures farther south show roughly the same shell size preferences at the warmer temperatures that we observed with the Massachusetts hermit crabs. If they do, it would suggest that as the climate continues to warm, the northern long-wristed hermit crabs will probably be found more consistently in smaller shells (for smaller individuals) and larger shells (for larger individuals). Hermit crabs have sometimes been observed to kill snails for their shells in the laboratory (Rutherford, 1977), but this is likely a rare occurrence (Laidre, 2011). Thus, hermit crabs are typically limited by the number of available empty shell options: on some beaches, small shells can be hard to come by (e.g., Pechenik et al., 2015a), while on others, large shells might be in short supply (e.g., Vance, 1972b). Thus, the effects of temperature shifts on shell size preferences would likely vary between locations.
Hermit crabs are constantly on the lookout for high-quality gastropod shells of appropriate size to use as shelters (Pechenik et al., 2001), and occupying inadequate shells could lead them to spend more of their time and energy finding (or fighting for) shells of better quality (McClintock, 1985). Our results indicate that the sizes of shells chosen by the hermit crab P. longicarpus at one temperature and salinity may differ from those preferred under altered conditions. Thus, whenever designing a study with hermit crabs of any species, it is important to ensure that the shells provided are of ideal size for the hermit crabs experiencing the given conditions. In addition, temperature and salinity should be closely monitored during any study to avoid unnecessary and potentially distracting fluctuations.
To summarize, we have shown that shifts in environmental temperature or salinity conditions can significantly alter the sizes of shells selected by the long-wristed hermit crab, P. longicarpus. Thus, it is important to ensure that future experiments requiring long-wristed hermit crabs to occupy shells of preferred size take temperature and salinity into account, because shell size preferences can apparently vary with changes in environmental conditions. Future studies will be needed to determine whether this reflects an adaptive shift in shell preference or a maladaptive shift in the ability of the hermit crabs to choose shells of the most appropriate size.
We thank Noah Epstein for help with experimentation and hermit crab care and two reviewers for their detailed and very helpful comments on an earlier draft of this manuscript.
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SARAH GILLIAND (*) AND JAN A. PECHENIK
Department of Biology, Tufts University, Medford, Massachusetts 02155
Received 3 March 2018; Accepted 10 August 2018; Published online 9 November 2018.
(*) To whom correspondence should be addressed. E-mail: firstname.lastname@example.org.
Table 1 Number and size of hermit crabs (Pagurus longicarpus) in each treatment, after gravid females and hermit crabs missing one or both of their chelipeds were discarded from the analysis Wet weight (mg) Treatment n Mean Median SD Control (22 [degrees]C, 30PPt) 35 478 352 298 16 [degrees]C. 30 ppt 34 323 251 248 32 [degrees]C, 30 ppt 42 490 314 333 22 [degrees]C. 15 ppt 44 320 240 285 22 [degrees]C, 20 ppt 35 364 277 241 22 [degrees]C, 40 ppt 46 293 234 235 SD, standard deviation.
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|Author:||Gilliand, Sarah; Pechenik, Jan A.|
|Publication:||The Biological Bulletin|
|Date:||Dec 1, 2018|
|Previous Article:||Observations on the Life History and Geographic Range of the Giant Chemosymbiotic Ship worm Kuphus polythalamius (Bivalvia: Teredinidae).|
|Next Article:||Permanently Fused Setules Create Unusual Folding Fans Used for Swimming in Cyprid Larvae of Barnacles.|