Donald C. Behringer

Ecology: Avoidance of disease by social lobsters

Transmissible pathogens are the bane of social animals, so they have evolved behaviours to decrease the probability of infection. There is no record, however, of social animals avoiding diseased individuals of their own species in the wild. Here we show how healthy, normally gregarious Caribbean spiny lobsters (Panulirus argus) avoid conspecifics that are infected with a lethal virus. Early detection and avoidance of infected, though not yet infectious, individuals by healthy lobsters confers a selective advantage and highlights the importance of host behaviour in disease transmission among natural populations.

Transmission of Panulirus argus virus 1 (PaV1) and its effect on the survival of juvenile Caribbean spiny lobster.

The Caribbean spiny lobster Panulirus argus, an important fisheries species, is host to Panulirus argus virus 1 (PaV1), a lethal, unclassified virus--the first found in any species of lobster--prevalent in juvenile lobsters. We describe a series of laboratory experiments aimed at assessing the likely modes of disease transmission, determining the survival of lobsters relative to each transmission pathway and identifying potential alternate hosts. Given evidence for lower prevalence of PaV1 in large lobsters, the effect of lobster size on susceptibility was also examined. Results demonstrated that PaV1 can be transmitted to juvenile lobsters via inoculation, ingestion of diseased tissue, contact with diseased lobsters and--among the smallest juveniles--through water over distances of a few meters. Contact and waterborne transmission, the most likely modes of transmission in the wild, were less efficient than inoculation or ingestion. Nevertheless, about half of the smallest lobsters in contact and waterborne trials contracted the disease and died within 3 mo. Other decapods that co-occur with P. argus (e.g. spotted lobster P. guttatus, stone crab Menippe mercenaria, channel crab Mithrax spinosissimus) did not acquire the disease after inoculation with PaV1-infected hemolymph. Our results confirmed that PaV1 is highly infectious and lethal to juvenile P. argus, particularly early benthic juveniles in the wild, and, hence, is a threat to mariculture.

Review of Panulirus argus virus 1--a decade after its discovery.

In 2000, a pathogenic virus was discovered in juvenile Caribbean spiny lobsters Panulirus argus from the Florida Keys, U.S.A. Panulirus argus virus 1 (PaV1) is the first naturally occurring pathogenic virus reported from lobsters, and it profoundly affects their ecology and physiology. PaV1 is widespread in the Caribbean with infections reported in Florida (U.S.A.), St. Croix, St. Kitts, Yucatan (Mexico), Belize, and Cuba. It is most prevalent and nearly always lethal in the smallest juvenile lobsters, but this declines with increasing lobster size; adults harbor the virus, but do not present the characteristic signs of the disease. No other PaV1 hosts are known. The prevalence of PaV1 in juvenile lobsters from the Florida Keys has been stable since 1999, but has risen to nearly 11% in the eastern Yucatan since 2001. Heavily infected lobsters become sedentary, cease feeding, and die of metabolic exhaustion. Experimental routes of viral transmission include ingestion, contact, and for newly settled juveniles, free virus particles in seawater. Prior to infectiousness, healthy lobsters tend to avoid diseased lobsters and so infected juvenile lobsters mostly dwell alone, which appears to reduce disease transmission. However, avoidance of diseased individuals may result in increased shelter competition between healthy and diseased lobsters, and greater predation on infected lobsters. Little is known about PaV1 outside of Mexico and the USA, but it poses a potential threat to P. argus fisheries throughout the Caribbean.

Stable isotope analysis of production and trophic relationships in a tropical marine hard-bottom community

Seagrasses produce much of the organic carbon in the shallow waters of the Caribbean and it has long been assumed that a substantial portion of this carbon is exported to nearby habitats, contributing substantially to their food webs. In the shallow coastal waters of the Florida Keys (USA), seagrass intersperses with hard-bottom habitat where bushy, red macroalgae are the most prominent primary producers. However, the relative importance of seagrass-derived carbon versus autochthonous algal production or phytoplankton in supporting higher trophic levels within hard-bottom communities has never been investigated. We compared the carbon and nitrogen isotopic values of potential primary producers and representative higher trophic level taxa from hard-bottom sites on the bay-side and ocean-side of the Florida Keys. We also included in our study a set of bay-side sites that experienced significant ecological disturbances over the past decade (e.g., cyanobacteria blooms, seagrass die-off, and sponge die-offs) that may have altered trophic relationships in those regions. We did not detect any differences among regions in the trophic status of hard-bottom taxa that might be associated with ecosystem disturbance. However, our results suggest that autochthonous production of algal detritus is an important source of secondary production in these hard-bottom communities, with seagrass and phytoplankton contributing smaller fractions.

Disease avoidance influences shelter use and predation in Caribbean spiny lobster

Shelter competition is uncommon among social animals, as is the case among normally gregarious Caribbean spiny lobsters (Panulirus argus). However, healthy lobsters avoid sheltering with conspecifics infected by a lethal pathogenic virus, PaV1. These contradictory behaviors have implications for shelter use and survival, especially in areas where shelter is limited. In laboratory experiments, we tested shelter competition between paired healthy and diseased juvenile lobsters in shelter-limited mesocosms. Neither healthy nor diseased lobsters dominated access to shelters, but lobsters shared shelter less often when diseased lobsters were present relative to controls with two healthy lobsters. We hypothesized that exclusion of juvenile lobsters from shelter results in increased mortality from predation, especially for the more lethargic, infected individuals. Field tethering trials revealed that predation was indeed higher on infected individuals and on all tethered lobsters deprived of shelter. We then tested in mesocosm experiments how the contrasting risks of predation versus infection by a lethal pathogen influence shelter use. Lobsters were offered a choice of an empty shelter or one containing a diseased lobster in the presence of a predator (i.e., caged octopus) whose presence normally elicits shelter-seeking behavior, and these data were compared with a previous study where the predator was absent. Lobsters selected the empty shelter significantly more often despite the threat of predation, foregoing the protection of group defense in favor of reduced infection risk. These results offer striking evidence of how pathogenic diseases shape not only the behavior of social animals but also their use of shelters and risk of predation.

Distribution, Prevalence, and Genetic Analysis of Panulirus Argus Virus 1 (Pav1) from the Caribbean Sea

The pathogenic virus Panulirus argus virus 1 (PaV1) was first discovered in Caribbean spiny lobsters Panulirus argus from the Florida Keys (USA) in 1999 and has since been reported in Belize, Mexico, and Cuba; its distribution in the wider Caribbean is unknown. We collected tissue samples from adult spiny lobsters from 30 locations in 14 countries bordering the Caribbean Sea and used molecular diagnostics to assay for the presence of PaV1. PaV1 occurred primarily in the northern areas of the Caribbean, where its prevalence was highest. The virus was not found in lobsters from the southeastern Caribbean, and its prevalence was lowest in the southwestern Caribbean. DNA sequence analysis was performed on a fragment of the viral DNA to examine the genetic diversity of PaV1 on a Caribbean-wide scale. Sequence variation in the viral DNA fragment was high, with 61 unique alleles identified from 9 areas. The sharing of viral alleles in lobsters from distant locations supports the hypothesis of a strong genetic connectivity among lobsters within the Caribbean, and further supports the hypothesis that postlarvae infected with PaV1 may serve to disperse the virus over long distances.

Is seagrass an important nursery habitat for the Caribbean spiny lobster, panulirus argus, in Florida?

Abstract Caribbean spiny lobster (Panulirus argus) settle preferentially in macroalgal‐covered hard‐bottom habitat, but seagrass is more prevalent in Florida (United States) and the Caribbean, so even low settlement of lobsters within seagrass could contribute substantially to recruitment if post‐settlement survival and growth were high. We tested the role of seagrass and hard‐bottom habitats for P. argus recruitment in three ways. We first explored possible density‐dependent regulation of early benthic juvenile lobster survival within cages deployed in seagrass and hard‐bottom habitats. Second, we compared settlement and survival of P. argus in both habitats, by comparing the recovery of microwire‐tagged early benthic juveniles from patches of seagrass and hard‐bottom. Finally, we assessed the relative abundance of juvenile lobsters in each habitat by deploying artificial structures in seagrass sites and compared these data with data from similar deployments of artificial structures in hard‐bottom habitat in other years. More early benthic juvenile lobsters were recovered from cages placed in hard‐bottom than in seagrass, but mortality of the early benthic life stage was high in both habitats. In regional surveys, the mean number of lobsters recovered from artificial shelters deployed within seagrass was lower than in any year that we sampled hard‐bottom, indicating that fewer lobsters reside naturally in seagrass, particularly large juveniles >40 mm carapace length. The greater abundance (and likely survival) of juvenile P. argus that we observed in hard‐bottom habitat as opposed to seagrass, combined with previous studies demonstrating that postlarval P. argus are attracted to, settle in, and metamorphose more quickly in red macroalgae, confirm that macroalgae‐dominated hard‐bottom habitat appears to be the preferred and more optimal nursery for Caribbean spiny lobster.

Sexual Dimorphism, Allometry, and Size at First Maturity of the Caribbean King Crab, Mithrax spinosissimus, in the Florida Keys

ABSTRACT The Caribbean King crab Mithrax spinosissimus is the largest brachyuran found in the western Atlantic and it supports subsistence and small commercial fisheries throughout the Caribbean and Gulf of Mexico. Because of its short larval duration and rapid growth, M. spinosissimus is considered a good candidate for aquaculture. Our study documents for the first time the size at sexual maturity, sexual dimorphism, and allometric growth relative to carapace width for certain secondary sexual characters in male and female M. spinosissimus from the Florida Keys, Florida. Using principal component analysis, K-means cluster analysis, and discriminant analysis, we identified 2 major growth phases in the postlarval benthic life of this species (juvenile or prepubertal and adult or pubertal). The typical growth pattern for majoid crabs includes a third, intermediate growth phase that appears absent in M. spinosissimus. The major cheliped of males was larger than that of females and exhibited positive allometric growth to maturity, after which the level of allometry decreased. In females, both chelipeds exhibited positive allometry throughout ontogeny. Abdominal width was negatively allometric throughout ontogeny in males, whereas in females the abdomen exhibited positive allometric growth until reproductive maturity, at which point it became isometric. Logistic regression indicated that the carapace width at first maturity was 45.2 mm in males and 69.7 mm in females. This new information should be taken into account when assessing stocks and setting harvest regulations if this fishery is to be managed sustainably.

Diseases of wild and cultured juvenile crustaceans: Insights from below the minimum landing size.

Decapod crustaceans (i.e., lobsters, crabs, and shrimps) are all subject to disease, both in the wild and in culture. No life stage appears to be immune to some form of pathogen or parasite. However, juveniles appear to be the targets of some of the most pervasive and consequential diseases. It is therefore surprising, given the enormous economic value of adult decapods, that we know so little about the effects of pathogens on their vulnerable life stage. Here I review the significant diseases reported for juvenile decapods that support fisheries and aquaculture, and highlight research that demonstrates the advantage of incorporating juveniles and ecology in studies of disease.

Disease effects on lobster fisheries, ecology, and culture: overview of DAO Special 6

Lobsters are prized by commercial and recreational fishermen worldwide, and their populations are therefore buffeted by fishery practices. But lobsters also remain integral members of their benthic communities where predator-prey relationships, competitive interactions, and host-pathogen dynamics push and pull at their population dynamics. Although lobsters have few reported pathogens and parasites relative to other decapod crustaceans, the rise of diseases with consequences for lobster fisheries and aquaculture has spotlighted the importance of disease for lobster biology, population dynamics and ecology. Researchers, managers, and fishers thus increasingly recognize the need to understand lobster pathogens and parasites so they can be managed proactively and their impacts minimized where possible. At the 2011 International Conference and Workshop on Lobster Biology and Management a special session on lobster diseases was convened and this special issue of Diseases of Aquatic Organisms highlights those proceedings with a suite of articles focused on diseases discussed during that session.