Effects of Cymatocarpus solearis (Trematoda: Brachycoeliidae) on its second intermediate host, the Caribbean spiny lobster Panulirus argus.

Many digenean trematodes require three hosts to complete their life cycle. For Cymatocarpus solearis (Brachycoeliidae), the first intermediate host is unknown; the Caribbean spiny lobster Panulirus argus is a second intermediate host, and the loggerhead turtle Caretta caretta, a lobster predator, is the definitive host. Trophically-transmitted parasites may alter the behavior or general condition of intermediate hosts in ways that increase the hosts' rates of consumption by definitive hosts. Here, we examined the effects of infection by C. solearis on P. argus by comparing several physiological and behavioral variables among uninfected lobsters (0 cysts) and lobsters with light (1-10 cysts), moderate (11-30 cysts), and heavy (>30 cysts) infections. Physiological variables were hepatosomatic index, growth rate, hemocyte count, concentration in hemolymph of cholesterol, protein, albumin, glucose, dopamine (DA) and serotonin (5-HT). Behavioral variables included seven components of the escape response (delay to escape, duration of swimming bout, distance traveled in a swimming bout, swim velocity, acceleration, force exerted, and work performed while swimming). There was no relationship between lobster size or sex and number of cysts. Significant differences among the four lobster groups occurred only in concentration of glucose (lower in heavily infected lobsters) and 5-HT (higher in heavily and moderately infected lobsters) in plasma. As changes in 5-HT concentration can modify the host's activity patterns or choice of microhabitat, our results suggest that infection with C. solearis may alter the behavior of spiny lobsters, potentially increasing the likelihood of trophic transmission of the parasite to the definitive host.

Artificial shelters and marine infectious disease: no detectable effect of the use of casitas to enhance juvenile Panulirus argus in shelter-poor habitats on a viral disease dynamics.

Casitas, low-lying artificial shelters that mimic large crevices, are used in some fisheries for Caribbean spiny lobsters (Panulirus argus). These lobsters are highly gregarious and express communal defense of the shelter. Scaled-down casitas have been shown to increase survival, persistence, and foraging ranges of juveniles. Therefore, the use of casitas has been suggested to help enhance local populations of juvenile P. argus in Caribbean seagrass habitats, poor in natural crevice shelters, in marine protected areas. Following the emergence of Panulirus argus virus 1 (PaV1), which is lethal to juveniles of P. argus, concern was raised about the potential increase in PaV1 transmission with the use of casitas. It was then discovered that lobsters tend to avoid shelters harboring diseased conspecifics, a behavior which, alone or in conjunction with predatory culling of diseased lobsters, has been proposed as a mechanism reducing the spread of PaV1. However, this behavior may depend on the ecological context (i.e., availability of alternative shelter and immediacy of predation risk). We conducted an experiment in a lobster nursery area to examine the effect of the use of casitas on the dynamics of the PaV1 disease. We deployed 10 scaled-down casitas per site on five 1-ha sites over a reef lagoon (casita sites) and left five additional sites with no casitas (control sites). All sites were sampled 10 times every 3-4 months. Within each site, all lobsters found were counted, measured, and examined for clinical signs of the PaV1 disease. Mean density and size of lobsters significantly increased on casita sites relative to control sites, but overall prevalence levels remained similar. There was no relationship between lobster density and disease prevalence. Dispersion parameters (m and k of the negative binomial distribution) revealed that lobsters tended to avoid sharing natural crevices, but not casitas, with diseased conspecifics. These results confirm that casitas provide much needed shelter in seagrass habitats and that their large refuge area may allow distancing between healthy and diseased lobsters. On eight additional sampling times over two years, we culled all diseased lobsters observed on casita sites. During this period, disease prevalence did not decrease but rather increased and varied with site, suggesting that other factors (e.g., environmental) may be influencing the disease dynamics. Using scaled-down casitas in shelter-poor habitats may help efforts to enhance juvenile lobsters for conservation purposes, but monitoring PaV1 prevalence at least once a year during the first few years would be advisable.

Do ecological characteristics drive the prevalence of Panulirus argus virus 1 (PaV1) in juvenile Caribbean spiny lobsters in a tropical reef lagoon?

PaV1 is a pathogenic virus found only to infect Caribbean spiny lobsters Panulirus argus, a major fishing resource. P. argus is a benthic mesopredator and has a complex life history, with several ontogenetic habitat changes. Habitat characteristics and species diversity of surrounding communities may have implications for disease dynamics. This is of more concern for juvenile lobsters, which are more susceptible to PaV1 and are far less mobile than adult lobsters. We targeted a population of juvenile P. argus in a reef lagoon in Mexico, where PaV1 was first observed in 2001. Prevalence has been since irregularly assessed, but in 2016 we began a more systematic assessment, with two sampling periods per year (June and November) in three different zones of the reef lagoon. To examine the relationship between PaV1 prevalence and potential ecological determinants, we assessed habitat complexity, cover of different substrates, and invertebrate community composition in all zones during the first four sampling periods (June and November 2016 and 2017). Habitat complexity and percent cover of some substrates varied with zone and sampling period. This was the case for seagrass and macroalgae, which nevertheless were the dominant substrates. The invertebrate community composition varied with sampling period, but not with zone. Probability of infection decreased with increasing lobster size, consistent with previous studies, but was not affected by zone (i.e., variations in ecological characteristics did not appear to be sufficiently large so as to influence prevalence of PaV1). This result possibly reflects the dominance of marine vegetation and suggests that lobsters can be sampled throughout the reef lagoon to assess PaV1 prevalence. Prevalence was higher in only one of seven sampling periods (November 2017), suggesting that the pathogen has leveled off to an enzootic level.

Variability in clinical prevalence of PaV1 in Caribbean spiny lobsters occupying commercial casitas over a large bay in Mexico.

In Bahía de la Ascensión, Mexico, the fishery for spiny lobsters Panulirus argus is based on the extensive use of casitas, large artificial shelters that can harbor the full size range of these highly gregarious lobsters. The discovery of a pathogenic virus in these lobsters (Panulirus argus virus 1, or PaV1) has raised concern about its potential effects on casita-based fisheries. Because in Bahía de la Ascensión visibly infected lobsters represent an immediate loss of revenue, we examined variability in clinical prevalence of PaV1 (percentage of lobsters visibly infected) in thousands of lobsters sampled from the commercial catch at the onset of 3 consecutive fishing years, and from 530 casitas distributed over 3 zones within the bay during 2 fishing and 2 closed seasons. In the commercial catch (lobsters 67 to 147 mm carapace length [CL]), clinical prevalence of PaV1 was low and was not affected by year or sex. In lobsters (9.2 to 115.0 mm CL) that occupied casitas, clinical prevalence of PaV1 varied with sampling season and was always higher in juveniles than in subadults or adults, but was consistently lower in one zone relative to the other 2 zones. The average clinical prevalence of PaV1 in this bay was statistically similar to the average clinical prevalence reported in Cuba, where casitas are also used, and in Florida Bay, USA, where casitas are not used. To date, PaV1 has had no discernible impact on the lobster fishery in Bahía de la Ascensión, suggesting that clinical prevalence is not influenced by the use of casitas per se.

Influence of local habitat features on disease avoidance by Caribbean spiny lobsters in a casita-enhanced bay.

In Bahía de la Ascensión, Mexico, 'casitas' (large artificial shelters) are extensively used to harvest Caribbean spiny lobsters Panulirus argus. After the discovery of a pathogenic virus, Panulirus argus virus 1 (PaV1), in these lobsters, laboratory experiments revealed that PaV1 could be transmitted by contact and through water, and that lobsters avoided shelters harboring diseased conspecifics. To examine these issues in the context of casitas, which typically harbor multiple lobsters of all sizes, we examined the distribution and aggregation patterns of lobsters in the absence/presence of diseased conspecifics (i.e. visibly infected with PaV1) in 531 casitas distributed over 3 bay zones, 1 poorly vegetated ('Vigía Chico', average depth: 1.5 m) and 2 more extensively vegetated ('Punta Allen': 2.5 m; 'Los Cayos': 2.4 m). All zones had relatively high indices of predation risk. Using several statistical approaches, we found that distribution parameters of lobsters were generally not affected by the presence of diseased conspecifics in casitas. Interestingly, however, in the shallower and less vegetated zone (Vigía Chico), individual casitas harbored more lobsters and lobsters were actually more crowded in casitas containing diseased conspecifics, yet disease prevalence was the lowest in lobsters of all sizes. These results suggest that (1) investment in disease avoidance by lobsters is partially modulated by local habitat features, (2) contact transmission rates of PaV1 may be lower in nature than in the laboratory, and (3) water-borne transmission rates may be lower in shallow, poorly vegetated habitats more exposed to solar ultraviolet radiation, which can damage viral particles.

Enhancement of juvenile Caribbean spiny lobsters: an evaluation of changes in multiple response variables with the addition of large artificial shelters.

Shortage of natural crevice shelters may produce population bottlenecks in juvenile Caribbean spiny lobsters (Panulirus argus), a socially gregarious species. We conducted a field experiment to test enhancement of a local population of juvenile P. argus with the addition of artificial shelters ("casitas") that mimic large crevices (1.1 m(2) in surface area and 3.8 cm in height). Changes in density and biomass of juvenile lobsters 15-50 mm carapace length (CL) were assessed with a multiple before-after control-impact (MBACI) analysis. Separate analyses were also conducted on small (15-35 mm CL) and large (35.1-50 mm CL) juveniles to assess size-related effects. First, we carried out 13 lobster surveys on nine fixed 1-ha sites over a shallow reef lagoon ("before" period). Then, we deployed ten casitas in each of five sites and left four sites as controls, and conducted 22 further surveys ("after" period). Deployment of casitas resulted in a sixfold increase in juvenile density (76% contributed by small and 24% by large juveniles) and a sevenfold increase in biomass (40 and 60%, respectively). Capture-recapture results revealed that enhancement was achieved not by promoting individual growth but by increasing survival, persistence, and foraging ranges of small and large juveniles. Casitas both mitigated shortage of natural shelter and increased sociality, allowing for cohabitation of smaller, more vulnerable juveniles with larger conspecifics that have greater defensive abilities. Casitas may help enhance local populations of juvenile P. argus in Caribbean seagrass habitats, typically poor in natural crevice shelters. The use of MBACI and the simultaneous assessment of multiple interrelated response variables may be a powerful analytical approach to test shelter limitation in other species and to examine the function of structural habitat in other systems.