No olfactory recognition of shell disease in American lobsters, Homarus americanus.
KEY WORDS: olfaction, dominance, social behavior, shell disease, American lobster, Homarus americanus
Epizootic shell disease (ESD) is a serious issue facing inshore populations of American lobster, Homarus americanus (Milne Edwards), in southern New England (SNE) waters. The lesions indicative of general shell disease infection (impoundment shell disease) were first discovered on lobsters kept in high-density tidal impoundments (Hess 1937). In the wild lobster populations, there is a low-level endemic form of shell disease that occurs possibly as a result of injuries. In 1996, a new form, called ESD, was described for lobsters from Rhode Island and southern Massachusetts (Castro & Angell 2000, Cobb & Castro 2006, Glenn & Pugh 2006). ESD can be differentiated from other forms of shell disease through the pathology of the lesions. Smolowitz et al. (2005) confirmed that the pathology of the lesions differed from other shell disease types in that pillars of chitin remained, whereas degradation occurred in the other polymers in the carapace. Kunkel et al. (2012) discussed that lesions in impoundment shell disease are located at dermal gland canals, whereas ESD lesions are located on the plane between these canals. The complex bacterial community in ESD lesions has now been well characterized through several methods (Bell et al. 2012, Chistoserdov et al. 2012, Meres et al. 2012). Two bacterial species in particular, Aquimarina 'homaria' and 'Thalassobius' sp. are abundant in the lesions in wild ESD lobsters (Chistoserdov et al. 2012).
Castro et al. (2006) found a mean prevalence of more than 45% in the upper East Passage of Narragansett Bay in Rhode Island, with disease prevalence fluctuating seasonally with the molting season. Greatest prevalence is in the late fall, after the molt occurs, and the shells may still be soft. Most vulnerable are egg-bearing females, which molt least frequently and are distinct hormonally. Research on the behavioral effects of shell disease in H. americanus is limited. A tagging study showed no difference between diseased and healthy lobsters in migration distance or direction (Landers 2005). Time budgets of healthy and diseased lobsters showed that diseased lobsters spent significantly more time in contact with shelter materials, indicating a behavioral difference between healthy and shell-diseased individuals (Castro et al. 2005).
Lobsters with ESD were found to have higher levels of ecdysone (molting hormone) than nonshell-diseased lobsters, indicating the involvement of the endocrine system in the defense strategy (Laufer et al. 2005). Tarrant et al. (2012) found that the expression of several genes changed significantly with disease status. In animals showing signs of ESD, low arginine kinase expression in muscle indicates that lobsters may be compromised energetically. There was an elevated expression of ecdysteroid receptor in both muscle and hepatopancreas of shell-diseased lobsters, and increased cytochrome P450 enzymes, indicating that shell disease is associated with disruption of chemical metabolism and hormonal signaling (Tarrant et al. 2012). Homerding et al. (2012) found that lobsters from the eastern portion of Long Island Sound (ELIS) had compromised immune systems relative to lobsters from western Long Island Sound (WLIS) or from Maine, suggesting that differences in the immune status of lobsters could be a factor in the regional differences in disease prevalence (prevalence is significantly higher in ELIS than WLIS or Maine). Lobsters with ESD showed significant differences in plasma antimicrobial activity in plasma and hemocyte phagocytosis, oxidative burst in hemocytes, as well as bacterial load in the hemolymph. All these physiological disruptions could affect the chemical makeup of an individual's urine. Lobsters use urine in chemical communication (Atema & Steinbach 2007). This provides the possibility for olfactory recognition of a diseased animal.
Intraspecific avoidance of diseased animals could reduce the spread of the disease if it were transmitted from animal to animal through physical contact, such as that demonstrated by healthy Caribbean spiny lobsters (Panulirus argus, Latreille), which actively avoided individuals infected with P. argus virus 1, a lethal disease, even before the infected individual showed any symptoms of the disease (Behringer et al. 2006). The study concluded that chemical cues released by infected lobsters mediated the avoidance behaviors of healthy lobsters.
Lobsters use urine to send pheromones to conspecifics during fights (Breithaupt & Atema 2000). The urine signals are received by aesthetasc sensilla of the antennules (Johnson & Atema 2005) and serve in individual recognition (Karavanich & Atema 1998a, Karavanich & Atema 1998b), which is important in dominance relationships for both sexes. Male dominance, in turn, is related to mating success (Cowan & Atema 1990). Although premolt females preferred dominant males significantly (P = 0.01), intermolt females showed only a slight preference for dominant males (P = 0.07) (Bushmann & Atema 2000). In sum, lobsters use odor signals to recognize sex, dominance, and individuals.
Female lobster preference for males may be affected by shell disease. First, females could detect the presence of the disease and avoid males that emit that cue, similar to the phenomenon found in P. argus. Second, in the event healthy males are better capable of establishing dominance over diseased males, females may select indirectly for healthy individuals by preferring the dominant male. Third, healthy and diseased lobsters might belong to different subpopulations, which could be differentiated behaviorally such that females might prefer to associate with local males.
Because male dominance is important for female mate choice, an inability to gain dominance could affect reproductive success in diseased males negatively. Although females, with their longer intermolt stage, suffer greater disease incidence, a lack of healthy males (such as in diseased areas) may further depress local reproduction. Using premolt rather than intermolt females might increase their mate choice and might relate more directly to reproduction and disease transmission. However, it would be nearly impossible to have sufficient numbers of healthy premolt females available while at the same time having the right combination of size-matched healthy and diseased males from the same site. Therefore, we chose to work with size-matched, primarily intermolt males and females.
Our research was motivated by the fact that H. americanus relies on chemical signals to obtain information about its environment, prominently including its social environment (Atema & Steinbach 2007). The nephropore gland of the lobster contains glycoproteins, and its ducts lead into the urine bladder (Bushmann & Atema 1996). Lobster urine contains large amounts of proteins (100-300 mg/mL (McLaughlin et al. 1999)), which could serve as pheromones. The effects of shell disease on hemolymph protein levels or other metabolic disruptions (Floreto et al. 2000) could alter the chemical signals used by lobsters during mating or fighting, thus affecting behavioral responses.
Here we investigate the behavioral response of intermolt females when presented with the odor of a healthy versus a diseased male, both before and after the pair had established a dominance relationship. The effect of shell disease on male dominance was also evaluated.
MATERIALS AND METHODS
Lobsters for behavioral tests were collected from 2 sample locations in Rhode Island where ESD is prevalent; from the Upper East Passage area inside Narragansett Bay (referred to as the RIN population) or an adjacent 2 x 5-mi area outside the Bay in Rhode Island Sound (the RIS population). The sites are approximately 25 mi apart. Data collected for each lobster include carapace length (CL), sex, and degree of shell disease. Male lobster CL ranged from 77.5-88.5 mm in RIN and 82.6-85.5 mm in RIS, allowing for the formation of size-matched pairs (within 2 mm CL). Female CL ranged from 81.8-93.0 mm in RIN and 81.5-86.0 mm in RIS. Degree of ESD in males ranged from 40-80% of the shell surface exhibiting lesions; however, testing the effect of different degrees of shell disease was not within the scope of this study. Healthy males and females that showed signs of ESD and animals that molted were immediately removed from the experiment and replaced if a suitable replacement was available.
All behavioral experiments were conducted in fall 2008, winter 2009, and spring 2010 in the Boston University Marine Program Laboratory. Similar to natural conditions, temperature of the artificial seawater ranged from 15-17[degrees]C (mean, 16[degrees]C), salinity ranged from 32-33 ppt, and pH was held at a mean of 8.0. All lobsters were fed 3 times/wk on a diet of peeled shrimp, which was chosen to maintain water quality in the system. The experimental design required holding animals for long periods in the laboratory. Initially, male lobsters were separated into individual bins whereas female lobsters were kept together in larger tanks. Individual recognition experiments (Karavanich & Atema 1998a) showed that lobsters no longer recognize each other after 2 wk of separation. Thus, to avoid dominance and individual recognition effects in the first test series, we separated the males for at least 2 wk in individual holding bins after we obtained them.
For odor choice experiments we used a dimly lit, 2-channel flume containing 2 shelters upstream and 1 shelter downstream (Fig. 1). The flume measured 350 x 135 cm with a water depth of 28 cm upstream and 34 cm downstream. The mean flow was ~2 cm/sec, and was recirculated and filtered through activated carbon to reduce lingering scents. The males served as odor "donors" and for tests were held in the upstream shelters; the female was acclimated in the downstream shelter. A solid plastic barrier separated the upstream half of the flume; the downstream half had no barrier. Water passed through the male shelters and flowed down in 2 separate columns toward the female shelter, converging on a central drain behind the female's shelter (Fig. 1). Daily dye tests ensured that the 2 water masses remained unidirectional and distinct until reaching the female's shelter. The experimental design called for 2 test series: first when the males of a pair were unfamiliar with each other (naive) and, second, after they had established a dominance relationship.
To avoid the possibility that lobsters prefer to associate with conspecifics from their own site, females from each site were tested only with males from their own site. We tested the male pairs first before and then after they had established dominance. The experimental design allowed us to evaluate effects of disease, male dominance, and their interaction on female recognition and preference for male odors while avoiding effects of site preference. The behavioral experimental design called for the RIN and RIS populations to be tested separately, each with 10 size-matched male pairs (1 healthy, 1 with shell disease) evaluated by 10 healthy females. Difficulty of obtaining simultaneously the proper number of healthy and diseased males and females from the 2 sites led to 3 separate testing periods. During each period, several animals had to be replaced. A suitable replacement would be an animal of the same sex that was size matched, of the same disease condition, and from the same sample site as the individual to be replaced.
It was not always possible to obtain individuals from the proper site and in the proper condition when needed. Therefore, we chose to work with size-matched, primarily intermolt males and females. As a result, 10 male pairs from RIN and 8 from RIS were used as well as 30 RIN and 24 RIS females. Of the 10 RIN pairs, 5 were tested with 10 females (50 trials, n = 50), and the remaining 5 pairs with 5-8 females (33 trials, n = 33). A total of 83 trials were run using RIN individuals. The 8 RIS pairs all were tested with 10 females, resulting in a sample size of 80 trials. Combining the populations resulted in a sample size of 163 trials.
Initial testing was 2 males and 1 female in their respective shelters. After a 5-min acclimation period, during which the odor plumes emanating from the males were established, the trial began. The female's shelter was opened and lit by an overhead (40-W) light that encouraged her to leave. For 10 min, the location of the female within the flume was measured with the following distance criteria: time spent in her shelter (SH), in the open flume area (O, downstream of the central barrier), in the channel (C, past the central barrier but not within 30 cm of the male shelters), near (N, within 30 cm of a male shelter, but not trying to enter the shelter), and entering (E, actively attempting to enter the partially blocked shelter; Fig. 1). Thus, OCNE represents the summated time on either the left or the right side of the flume.
After 10 min, the female was coaxed gently back into her shelter and the males were switched between sides of the flume to account for inadvertent side bias. After a 5-min acclimation to reestablish the odor plumes and reacclimate the female, she was again released for an identical 10-min choice trial. For the subsequent test, the 2 males remained unchanged whereas the female was exchanged to repeat the same process until all available healthy females from the proper site were tested. We calculated trial results by combining the 2 parts of the test period. Using the statistical program JMP, a Wilcoxon's signed rank test was used to evaluate whether there was a significant difference between the time females spent within the odor plumes of the healthy or diseased males. No difference in time spent in either male's odor would be expected if females showed no preference for healthy or shell-diseased males.
After the naive trials were run with the entire female panel, each male pair was placed in an observation tank (size, 0.9 x 0.6 x 0.4 m). where they established dominance; we used dominance criteria adapted from Atema and Voigt (1995) and Karavanich and Atema (1998a). After the fight, the 2 males were held in the tank overnight for continuous contact and consolidation of the dominance relationship. The following day, the same female lobster panel was used to express possible preference for a member of the male pair postfight.
Regardless of distance criteria used in the analysis, there was no significant difference between the amount of time intermolt females from either population (RIN, RIS) or both populations combined (RIN + RIS) spent with pre- or postfight healthy and shell-diseased males (Table 1). The Wilcoxon's signed-rank values (W, H-SD) were predominantly positive, suggesting a trend toward preference for healthy males. In the post-RIN analysis, female enter attempts (E) showed a trend toward preference for healthy males (E: W = 68, P = 0.068). However, the latter result can be explained by a dominance effect.
Dominance was established by all 10 healthy RIN males and by 5 of the 8 RIS males; the other 3 dominant RIS males had shell disease (RIN + RIS, 2-tailed binomial test, P = 0.008). Females preferred dominant males by 1 criterion only: time spent trying to enter (E) dominant male shelters. Despite short durations of effort and a small sample size, this was significant for the RIS population (E: Tdom = 9, Tsub = 6; W, D-S = 114; P = 0.031), and nearly significant for the RIN population and the RIN and RIS populations combined (Table 2). The RIS females showed a trend toward healthy dominant males also for the OCNE criterion, for which the time values are more robust (OCNE: Tdom = 651, Tsub = 536; W, D-S = 364; P = 0.059). In the dominance analysis (Table 2), Wilcoxon's values were positive, except in the analysis of dominant, shell-diseased males (post-RIS, SD-Dom; n = 30), which indicated a slight female preference for healthy males. These results were not significant and did not affect our conclusion: Intermolt females do not prefer the odor of healthy or shell-diseased males. However, females do recognize male dominance odor as expressed in a small increase in entering attempts of the dominant male's shelter.
The results showed that intermolt female lobsters have no significant preference for healthy or shell-diseased males; both RIN and RIS females showed the same lack of preference. This suggests lack of disease recognition. The results are, in some respect, surprising, given that lobsters use odor for so many social situations. However, one can also conclude that the results are not surprising. Shell disease has been found in its current form only since 1997--a span of 2 lobster generations, a very short amount of time for any recognition and aversion to the disease to evolve. In addition, recognition of shell disease would not impact sexual selection if the disease was not spread through contact. Shell disease does affect the ability of male lobsters to establish dominance, as healthy males were dominant in 15 of 18 fights (P = 0.008). This could be explained easily by the physiological changes found by Tarrant et al. (2012) reflected in low arginine kinase expression in muscle tissue. Because the crusher claw, more than anything else, determines the outcome of dominance fights, a weakened crusher muscle would affect indirectly male competitiveness and, thus, evolutionary fitness.
At first, it seemed surprising that females did not prefer dominant healthy males more strongly to shell-disease subordinate males. However, females did not recognize shell disease, and their lack of significant preference for the dominant male has been seen earlier. Bushmann and Atema (2000) found that although premolt females preferred dominant males significantly (P = 0.01), intermolt females showed less than significant preference for dominant males (P = 0.07). Our current study showed a similar trend, favoring the dominant male in the criterion of entering attempts by RIN and RIS females (W = 240, P = 0.056; Table 2). Premolt females might have shown a much clearer preference for dominant males as they did in large communal tanks (mesocosms (Cowan & Atema 1990)) and in odor choice tests (Bushmann & Atema 2000). However, within our facilities and within the timeframe available for this study, it was impossible for the lobstermen to obtain the number of healthy premolt females (in summer) simultaneous with the required number of healthy and shell-disease intermolt males from each of the 2 study sites.
Nevertheless, the result that shell disease is not recognized by odor is robust. Lack of female preference for healthy males in both RIN and RIS populations was abundantly clear; they spent exactly the same amount of time in the odor areas of healthy and diseased males no matter where in the choice tank and no matter how we tried to identify individual female differences. This is expected from intermolt females and males from the same site. Even the small but significant preference of females to enter the dominant's shelter corresponds to earlier results with intermolt animals.
The other result, that shell-disease males lose fights and have problems establishing dominance, is also robust, and suggests indirect negative consequences for reproduction. In addition, shell-disease males molt more frequently than healthy males, and it may take several postmolt months before their shell hardens sufficiently to start winning fights again (Cowan & Atema 1990). Thus, molting as well as shell disease put lobsters further down in the dominance order. This suggests that shell-disease males have fewer mating opportunities. In a reduced population such as exists currently in SNE, this could lead to a scarcity of suitable males to provide the reproductive input needed to build and maintain a healthy population. This male effect compounds the direct loss of ovigerous females from the population caused by their long intermolt, egg-bearing period that allows shell disease to flourish to a lethal level.
Highly contagious diseases have been shown to drive disease recognition mechanisms in spiny lobsters (Behringer et al. 2006). We did not identify an avoidance behavior in female intermolt lobsters in this research. We did identify an indirect effect of shell disease: diseased males lose fights. Female recognition and preference for dominant males could put shell-disease, and therefore likely subordinate, males at a mating disadvantage, thereby reducing the number of reproductive males and suppressing population growth.
This work was supported by the National Marine Fisheries Service as the New England Lobster Research Initiative: Lobster Shell Disease under NOAA grant NA06NMF4720100 to the University of Rhode Island Fisheries Center. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its subagencies. The U.S. government is authorized to produce and distribute reprints for government purposes, notwithstanding any copyright notation that may appear hereon. We thank Tom Angell of the Rhode Island Department of Environmental Management, Marine Fisheries Section of the Division of Fish and Wildlife for lobster sample collection; and Justin Scace and Jonathan Perry of the Boston University Marine Program for their technical assistance with the flume. The Boston University Marine Program and the environmental Systems Laboratory at Woods Hole Oceanographic Institution provided space to conduct experiments and hold animals. The Shell Disease Initiative was expertly led by Dr. Kathy Castro and Barbara Somers.
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* Corresponding author. E-mail: firstname.lastname@example.org
NATHAN RYCROFT, (1) * KRISTIN RADCLIFFE, (1) ERIN MCDOUGAL, (1) JULIA HALVERSON, (1) GABRIELE GERLACH, (2) JANA DEPPERMANN (2) AND JELLE ATEMA (1)
(1) Biology Department and Marine Program, Boston University, 5 Cummington St., Boston, MA 02215;
(2) University of Oldenburg, Department of Biodiversity and Evolution of Animals, Carl yon Ossietzky St 9-11 2622, Oldenburg, Germany
TABLE 1. Shell disease odor recognition: results and statistical evaluation. H/SD n Flume H (s) SD (s) Area PRE-RIN 83 OCNE 552 [+ or -] 27 592 [+ or -] 27 (10 male pairs) CNE 314 [+ or -] 28 352 [+ or -] 33 NE 203 [+ or -] 23 243 [+ or -] 29 E 12 [+ or -] 4 8 [+ or -] 3 PRE-RIS 80 OCNE 638 [+ or -] 24 562 [+ or -] 24 (8 male pairs) CNE 399 [+ or -] 28 340 [+ or -] 27 NE 294 [+ or -] 27 258 [+ or -] 26 E 17 [+ or -] 5 14 [+ or -] 4 PRE-(RIN + RIS) 163 OCNE 594 [+ or -] 18 577 [+ or -] 18 (18 male pairs) CNE 356 [+ or -] 20 346 [+ or -] 21 NE 248 [+ or -] 18 250 [+ or -] 20 E 15 [+ or -] 3 11 [+ or -] 3 POST-RIN 83 OCNE 567 [+ or -] 28 594 [+ or -] 27 (10 male pairs) CNE 336 [+ or -] 33 346 [+ or -] 33 NE 221 [+ or -] 28 230 [+ or -] 28 E 24 [+ or -] 7 13 [+ or -] 4 POST-RIS 80 OCNE 634 [+ or -] 29 558 [+ or -] 29 (8 male pairs) CNE 347 [+ or -] 33 286 [+ or -] 30 NE 259 [+ or -] 31 200 [+ or -] 26 E 9 [+ or -] 3 6 [+ or -] 2 POST-(RIN + RIS) 163 OCNE 600 [+ or -] 20 576 [+ or -] 20 (18 male pairs) CNE 342 [+ or -] 23 317 [+ or -] 22 NE 240 [+ or -] 21 215 [+ or -] 19 E 17 [+ or -] 4 9 [+ or -] 2 H/SD Flume W (H-SD) P Area (s) PRE-RIN OCNE -95 0.6 (10 male pairs) CNE -81 0.6 NE -110 0.5 E 22 0.5 PRE-RIS OCNE 309 0.12 (8 male pairs) CNE 280 0.18 NE 177 0.4 E 132 0.3 PRE-(RIN + RIS) OCNE 423 0.5 (18 male pairs) CNE 331 0.5 NE -91 0.9 E 251 0.2 POST-RIN OCNE -92 0.6 (10 male pairs) CNE 11 0.9 NE 1 1 E 68 0.068 POST-RIS OCNE 270 0.16 (8 male pairs) CNE 262 0.19 NE 245 0.2 E 16 0.8 POST-(RIN + RIS) OCNE 414 0.5 (18 male pairs) CNE 506 0.3 NE 481 0.3 E 188 0.14 Female preference for healthy (H) versus shell diseased (SD) males by population site (RIN, RIS, RIN + RIS combined) and by experimental phase (pre-and postfight), each with sample size of male pairs. n, number of female choice trials; flume areas, defined in text; H and SD, mean time females spent on side of healthy versus shell-diseased male (in seconds [+ or -] SEM); RIN, Upper East Passage area inside Narragansett Bay; RIS, adjacent 2 x 5-mi. area outside the bay in Rhode Island Sound; W (H-SD), Wilcoxon's signed rank; P, significance (in bold type, 0.05 < P < 0.1). Flume areas defined in text. TABLE 2. Dominance odor recognition in postfight phase: results and statistical evaluation. Dom/Sub n Flume Dom (s) Sub (s) Area Post-RIN 83 OCNE 567 [+ or -] 28 594 [+ or -] 27 (10 male pairs) CNE 336 [+ or -] 33 346 [+ or -] 33 NE 221 [+ or -] 28 230 [+ or -] 28 E 24 [+ or -] 7 13 [+ or -] 4 Post-RIS 80 OCNE 662 [+ or -] 29 538 [+ or -] 29 (8 male pairs) CNE 371 [+ or -] 36 269 [+ or -] 28 NE 279 [+ or -] 33 186 [+ or -] 24 E 9 [+ or -] 3 6 [+ or -] 2 Post-(RIN + RIS) 163 OCNE 597 [+ or -] 20 579 [+ or -] 20 (18 male pairs) CNE 337 [+ or -] 23 321 [+ or -] 22 NE 239 [+ or -] 21 216 [+ or -] 19 E 16 [+ or -] 4 10 [+ or -] 2 H-Dom Post-(RIN + RIS) 133 OCNE 609 [+ or -] 22 561 [+ or -] 22 (15 male pairs) CNE 352 [+ or -] 27 300 [+ or -] 24 NE 250 [+ or -] 24 201 [+ or -] 21 E 20 [+ or -] 5 9 [+ or -] 2 Post-RIS 50 OCNE 651 [+ or -] 41 536 [+ or -] 42 (5 male pairs) CNE 365 [+ or -] 45 278 [+ or -] 39 NE 286 [+ or -] 44 196 [+ or -] 32 E 9 [+ or -] 4 6 [+ or -] 2 SD-Dom Post-RIS 30 OCNE 594 [+ or -] 37 606 [+ or -] 37 (3 male pairs) CNE 289 [+ or -] 51 312 [+ or -] 50 NE 210 [+ or -] 47 215 [+ or -] 43 E 7 [+ or -] 3 8 [+ or -] 5 Dom/Sub Flume W (D-S) P Area (s) Post-RIN OCNE -92 0.6 (10 male pairs) CNE -11 0.9 NE -1 1 E 68 0.068 Post-RIS OCNE 364 0.059 (8 male pairs) CNE 223 0.3 NE 239 0.2 E 114 0.031 * Post-(RIN + RIS) OCNE 242 0.7 (18 male pairs) CNE 183 0.7 NE 210 0.7 E 240 0.056 H-Dom Post-(RIN + RIS) OCNE 283 0.5 (15 male pairs) CNE 273 0.5 NE 277 0.4 E 176 0.063 Post-RIS OCNE 139 0.17 (5 male pairs) CNE 105 0.3 NE 109 0.2 E 26 0.4 SD-Dom Post-RIS OCNE -17 0.7 (3 male pairs) CNE -45 0.4 NE -39 0.4 E -6 0.6 Dom-Sub, female preference for dominant versus subordinate males; Dom and Sub, mean time females spent on side of dominant versus subordinate male (in seconds [+ or -] SEM); H-Dom and SD-Dom, as previous, but separated by pairs where healthy (H) male or shell- disease (SD) male was dominant. RIN, Upper East Passage area inside Narragansett Bay; RIS, adjacent 2 x 5-mi. area outside the bay in Rhode Island Sound. Note: In the RIN population, all healthy males were dominant, so no SD-Dom category.) See also Table 1. Flume areas defined in text. (Bold type, 0.05 < P < 0.1; asterisk, p < 0.05).
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|Author:||Rycroft, Nathan; Radcliffe, Kristin; McDougal, Erin; Halverson, Julia; Gerlach, Gabriele; Deppermann|
|Publication:||Journal of Shellfish Research|
|Date:||Jun 1, 2012|
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