The 1999 Long Island Sound Lobster mortality event: findings of the comprehensive research initiative.

ABSTRACT In 1999, the Long Island Sound lobster fishery suffered a significant mortality event, following 2 years of smaller, more localized, die-offs. A national research initiative investigating the potential cause(s) of the mortalities was undertaken under the auspices of the Steering Committee for Lobster Disease Research, a subcommittee of the Atlantic States Marine Fisheries Commission's Lobster Management Board. More than 20 research efforts investigated the effects of anthropogenic and environmental stressors and disease on lobsters over a 3-year period. The findings of the collective projects were synthesized and presented publicly in October 2004. Lobsters, at an all-time high abundance, and possibly already infected with parasitic amoebae, Neoparamoeba pemaquidensis, were subjected to sustained, stressful environmental conditions, driven by above average water temperature. Physiologically weakened and unable to fend off disease (paramoebiasis), many lobsters died.

KEY WORDS: lobster, mortality, Long Island Sound, disease, pesticides, paramoeba, temperature, Homarus americanus

INTRODUCTION

During the fall of 1999, the American lobster (Homarus americanus H. Milne Edwards, 1837) population in Long Island Sound (LIS) suffered a significant mortality event, particularly in the western and central Sound. Bistate (Connecticut and New York) commercial lobster landings from western LIS (west of Norwalk, Connecticut) declined by as much as 99% from the previous year, and reductions of landings for ports east of Norwalk ranged from 64% to 91% (CTDEP 2000). At the same time, lobstermen in eastern LIS (as well as Rhode Island and Massachusetts) continued to see a rise in the incidence and extent of shell disease in lobsters, which, while apparently unrelated to the mortality event, raised additional concerns about the status and health of the lobster resource and the Long Island Sound commercial fishery.

In late September, the Connecticut Department of Environmental Protection (CTDEP) collected water samples for analysis and contracted with the University of Connecticut to test the samples for a range of materials including pesticides, herbicides, PCBs, semivolatile organic compounds, volatile organic compounds, heavy metals and cyanide. The test results were negative. If pesticides or any other of these materials were present, their concentration levels were less than the parts-per-billion detection limits of the analytical equipment used (CTDEP 2000, DeFur 2000). Samples were also provided to the National Marine Fisheries Service Laboratory in Milford, Connecticut to screen for toxic phytoplankton and bacteria. None were found.

Lobster specimens were sent to the University of Connecticut for gross and histopathologic examination in mid October. By November, the pathology reports indicated that most lobsters examined were infected with what is now known as a strain(s) of the parasitic amoeba, Neoparamoeba pemaquidensis, a facultative pathogen of salmon and sea urchins (French 2000a, 2000b, CTDEP 2000, Mullen et al. 2005). Similar amoebae have caused fatal diseases in crustaceans at other times (e.g., grey crab disease). The parasitic amoebae infecting much of the nervous tissue of lobsters were considered to be the proximate cause of death of the lobsters, but it was unclear whether other factors played a role, setting the lobsters up for infection or suppressing any possible immune response to the infection (French 2000a, 2000b).

During the summer and fall of 1999, the mosquito-borne West Nile Virus (WNV) appeared for the first time in New York and Connecticut. By early September, seven human deaths had been attributed to complications due to WNV. Control programs were undertaken in both states to curb adult and larval mosquito populations. Application methods and pesticides used varied geographically as well as temporally, spanning an interval from early August to mid October, with maximum applications occurring during the last 2 weeks of September (Miller et al. 2005, Wilson et al. 2005, K. Chytalo, NYSDEC, pers. comm.). Malathion was applied in New York only, while pyrethroids (resmethrin and sumithrin) and methoprene were used in both states.

Early on, some lobstermen expressed concern about the apparent coincidental timing of the lobster mortalities, rain events and the application of these pesticides. Local associations of lobstermen retained biologists from the Lobster Institute in Maine to help in the initial investigation of the mortalities during the fall 1999.

By late 1999, the Governors of Connecticut and New York had requested disaster assistance from (then) United States Secretary of Commerce, William M. Daley (CTDEP 2000). On January 26, 2000, Secretary Daley declared the lobster fishery in LIS a "commercial fishery failure due to a resource disaster" under section 312(a) of the Magnuson-Stevens Fishery Conservation and Management Act (US Department of Commerce 2000, CTDEP 2000). Within 6 months, $13.9 million of federal disaster relief funds were authorized to provide economic relief for lobstermen and to support research to investigate the potential cause(s) of the mortality event; $6.6 million was designated for research and $7.3 million for economic relief. (These funds were appropriated in 2001.) The State of Connecticut also authorized bonding to provide $1 million for economic relief and about $1 million for research.

In April 2000, the first LIS Lobster Health Symposium was held in Stamford, CT. This meeting, organized by the Sea Grant programs in CT and NY on behalf of a bistate advisory committee, brought together lobstermen, researchers, resource managers, and others to discuss the mortality event, review the results of preliminary assessments, share observations and, absent a definitive cause of the deaths, develop a comprehensive list of potential causative factors for further investigation. The research priorities identified included resource assessment, pathology and anthropogenic inputs, as well as oceanographic and environmental processes (Balcom 2000). Efforts were also made to develop a time line for various events the previous fall.

The Atlantic States Marine Fisheries Commission (ASMFC) formalized the bistate advisory committee by establishing it as a subcommittee of its Lobster Management Board in August 2000. Known as the Steering Committee for Lobster Disease Research (SCLDR), its primary responsibilities were to guide the research initiative, recommend the allocation of available funds, and report back to the ASMFC Lobster Management Board. Appointed members represented NOAA Fisheries, NOAA National Sea Grant, CT and NY Sea Grant, the US Environmental Protection Agency (EPA), ASMFC, CTDEP, the New York State Department of Environmental Conservation (NYSDEC) and the LIS lobster industry. Under the guidance of the SCLDR, NOAA Fisheries allocated some funds to the states to enhance and expand their lobster population monitoring and assessment programs. The remaining funds were divided among NOAA Fisheries and the CT and NY Sea Grant programs to support research and extension work. Oversight of the $1 million State of Connecticut research fund was carried out by the CTDEP Office of Long Island Sound Programs.

A joint request for proposals was issued nationally by the Sea Grant programs and CTDEP in fall 2000. Researchers were asked to propose work in one of several areas: physical/chemical environment, disease, pesticides and immunological responses to stress. Extensive written peer reviews were obtained for all proposals. An international scientific advisory committee was convened to further review the proposals and the peer reviews and make recommendations. Final funding recommendations were made by the SCLDR. By July 2001, 17 research projects were underway, involving more than 30 institutions and agencies nationwide and, ultimately, more than 65 researchers and graduate students. Several additional research efforts were initiated in subsequent years.

The individual research projects took 2 to 3 years for completion. However, these results were not generated in isolation. During this period, two working meetings of the entire research initiative community were held to share and discuss preliminary results, and encourage cross-project collaborations as appropriate. Additional LIS lobster health symposia were held in Ronkonkoma, New York (2002) and Bridgeport, Connecticut (2003), providing updates on the progress of the research initiative to the lobstermen, press, and public.

Several unresolved key questions for the SCLDR were just how much of each of the mosquito-control pesticides was applied, when, and where, and was it enough to cause mass mortality of lobsters. Obtaining access to the pesticide application data, protected by law in New York in particular, was a long and difficult process, delaying the SCLDR's ability to fully address these questions until the summer of 2004.

To compare the laboratory-derived lethal and sublethal endpoints for three of the pesticides with actual conditions in LIS in 1999, the SCLDR supported two independent modeling efforts in 2004 using existing hydrodynamic models and actual pesticide loadings from 1999 (Miller et al. 2005, Wilson et al. 2005). The objective was to investigate whether the quantity of individual pesticides applied over time to control mosquitoes could, alone, have been responsible for the lobster mortalities. Following the guidance of the SCLDR pesticide subcommittee, the modeling exercises conservatively focused on a "worst case scenario," making a "Phase I" assumption that the entire amount of a pesticide applied in an area reached the water and did not eventually decay. "Phase II" assumptions were also very conservative, assuming that 100% of the individual pesticides applied entered the water (no degradation in the air or on land, and no adherence to soil particles), and then decayed according to set rates.

Collective results of the research initiative were announced and discussed during the Fourth LIS Lobster Health Symposium (Stony Brook, New York) in October 2004. Findings of individual projects were integrated and presented during 5 "topical" presentations on resource monitoring and assessment, physical/chemical environment, disease, pesticides and immunological responses to stress (McKown et al. 2004, Cuomo et al. 2004, Frasca et al. 2004, De Guise et al. 2004b, Dove et al. 2004). Results of one pesticide modeling exercise were presented (Miller 2004). A "neutral party" unaffiliated with the research initiative was retained by the SCLDR to synthesize the pertinent findings and present overall conclusions about the cause of the mortality event in 1999 (Pearce 2004).

The findings on which the conclusions presented at the October 2004 symposium and described in this study are based, were collectively discussed, and to a large degree, agreed upon by the researchers and SCLDR members in attendance at the second working meeting of the researchers held in Groton, CT in May 2004. (1) During that meeting, results of individual projects were shared, and findings that helped answer the question, "What happened to the lobsters in 1999?" were synthesized and are presented in this article.

FINDINGS

Early Signs of Trouble

From the mid 1990s onward, and particularly from 1996 to 1998, the abundance of lobsters in LIS was at an all-time high, as demonstrated by CTDEP trawl survey indices as well as the CT and NY commercial landings (CTDEP 2000, LoBue et al. 2003, Balcom 2003, Howell et al. 2005). CTDEP and NYSDEC phone logs, data from mail surveys of lobstermen in 1999 and 2000 and comments made by lobster industry panelists during the First LIS Lobster Health Symposium all indicate that smaller lobster mortality events occurred during 1997 and 1998 in western LIS from Norwalk to Greenwich, CT (CTDEP 2000, Frate 2000, Burt 2000, Doll 2000).

Even as early as November 1995, lethargic lobsters were reported to CTDEP by the director of the CT Department of Agriculture, Bureau of Aquaculture (E. Smith, CTDEP, E-mail comm.). Greater-than-normal numbers of lobsters were reported dead in fall of 1997 in western LIS, west of Greenwich (CTDEP 2000). One dealer reported having quality problems with LIS lobsters since July 1998 when lobsters began dying in his holding tanks and those of his customers (Burt 2000).

During fall 1998 and spring 1999, CT lobstermen reported that catches of lobsters in the waters off Stamford and Greenwich were largely nonexistent, although lobsters were found further east near Darien (CTDEP 2000, Frate 2000). From Stamford and Greenwich westward, atypical numbers of lobster mortalities were reported in fall 1998, though they did not approach the levels of 1999 (E. Smith, CTDEP, E-mail comm.).

Dead and Dying Lobsters

Western LIS lobstermen began reporting lethargic, moribund, and dead lobsters to the CTDEP and the NYSDEC beginning in late August and early September 1999 through phone calls and personal contacts (CTDEP 2000, unpublished transcripts of First LIS Lobster Health Symposium 2000). The reports focused on lobsters, but also included blue crabs, rock crabs, spider crabs, sea urchins and starfish. A few reports of lethargic and dead lobsters were received during September and October from eastern LIS lobstermen and from citizens in the Groton to Niantic (Connecticut) area who found dead lobsters on local beaches as well (CTDEP 2000). Lobstermen noted that it was sometimes difficult to distinguish between healthy and sick lobsters, except for those that were noticeably limp and/or lethargic. Reports continued throughout the fall until lobstermen ceased fishing when the catches did not justify the effort and expense, and pulled their traps.

Industry panelists at the LIS Lobster Health Symposium in 2000 described their experiences with the die-off, demonstrating that some experienced the problem sooner than others. For example, lobstermen trapped lobsters near Stamford and Greenwich for about 6 weeks during the summer of 1999. However, following a rainstorm of nearly two inches in mid-August, the lobsters disappeared (Frate 2000). When the lobsters did return, they were one-tenth the abundance the lobstermen were used to seeing, and some were dead in the traps (Frate 2000). During August, the presence of numerous blue crabs in deep water was also noted for the first time (Frate 2000).

Another lobsterman observed that a few days after a significant rainstorm in late August/early September, he hauled empty traps and traps with dead lobsters in the Norwalk (Connecticut) area (Makowsky 2000). In New York, from Lloyd's Neck to Prospect Point, regular catches of lobsters were caught the week of September 14th, until Tropical Storm Floyd came through the region on the 16th. The following Monday, September 20th, the lobster catch dropped by more than 75%, and dead lobsters appeared in the traps (Finke 2000). Landings remained low and more dead lobsters were found. In mid October, dealers complained that a tremendous number of LIS lobsters were arriving at their facilities properly cooled, but dead, with more dying within days (Finke 2000).

In late September or early October, new-shell lobsters were caught near Darien (Connecticut); however, the ratio of dead newshell lobsters trapped to live ones was 5 to 1 (Frate 2000). Alarmingly, some berried female lobsters were observed prematurely shedding their shells (Crismale 2000, Doll 2000).

Connecticut lobstermen fishing the central Sound delayed setting their traps from a normal late September time frame until mid October. Few lobsters were hauled, including dead ones (Crismale 2000). The fall run did not materialize during 1999, and the fall molt was delayed (CTDEP 2000). One industry panelist commented that it was obvious something catastrophic happened in September or October, but he believed that there was a buildup to it, that something had been going on for some time (Doll 2000). Another panelist said that the 1999 environmental conditions created a situation that ended up being a worst case scenario, and related it to how stressed and susceptible lobsters in his tanks become when the water warms or the ammonia level spikes (Burr 2000).

Warm Waters

Although lobsters inhabit the eastern coast of North America from northern Labrador to North Carolina (Herrick 1911), in terms of significant commercial fisheries, LIS marks the southernmost end of the inshore range of American lobsters (Stewart 1972, Lawton & Lavalli 1995). Juvenile and adult lobsters live in environments where the annual range in water temperature can be as little as 5[degrees]C or as much as 20[degrees]C (Aiken & Waddy 1986) with an optimal temperature range determining locations of greatest abundance (Stewart 1972). Temperature is one of the dominant physiochemical parameters that strongly influence the physiological and ecological properties of estuarine species; more than any other environmental parameter, temperature affects the growth, reproduction, rate of metabolic functions, and survival of lobsters (Kinne 1970, Prosser 1973, Cobb 1976, Aiken & Waddy 1986, Mercaldo-Allen & Kuropat 1994). Depending on acclimation temperature, and under optimal dissolved oxygen and salinity conditions, pre-adult lobsters have a broad thermal tolerance ranging from -1[degrees]C to 30.5[degrees]C, and can withstand abrupt temperature changes (McLeese 1956, Cooper & Uzmann 1980, Aiken & Waddy 1986). However, Stewart (1972) reported that normal lobster movement and behavior near Ram Island (Connecticut) was inhibited at a maximum bottom temperature of 18.9[degrees]C. Recent work on LIS lobsters showed that as water temperature was increased beyond a threshold of about 20.5[degrees]C, the respiration rate of lobsters increased significantly and the animals began to become stressed (Powers et al. 2004, Chang 2004, Dove et al. 2005).

Historical records show that, over the long-term, temperatures for the LIS region are increasing (Varekamp et al. 2004). The winter of 1998 to 1999 was warmer than average, and bottom water temperatures were atypically 1[degrees]C to 2[degrees]C warmer for a sustained period (Gates 2000). Data from a CTDEP water quality monitoring station near Hempstead, New York indicate that bottom waters in far western LIS never went below 3[degrees]C that winter; typically the temperature drops to 0[degrees] to 1[degrees]C (Gates 2000).

Water temperatures remained elevated through the spring and summer of 1999. Data from August 2 showed that bottom waters were slightly more than 21[degrees]C, and, in some well-mixed areas less than 20 m deep, exceeded 23.5[degrees]C (Wilson et al. 2004, Wilson & Swanson 2005). Basin-averaged bottom water temperatures were the highest for the decade during the months of July and August (Wilson & Swanson 2005). Overall that summer, temperatures at many CTDEP bottom water quality monitoring stations exceeded 20[degrees]C from early August through early October (CTDEP 1999). During the September CTDEP water quality monitoring cruise, bottom water temperatures at all stations were greater than 20[degrees]C; many approached or exceeded 22[degrees]C (CTDEP 1999).

CTDEP compared data from 2 stations, one 30 m deep in western LIS and the other 70 m deep in eastern LIS, and found that bottom water temperature at the western station exceeded the 20[degrees]C upper temperature tolerance threshold for American lobsters in 1999 for a total of 83 "stress degree days" (Simpson 2000). (2) The easternmost station near the Race experienced two "stress degree days" during 1999; normally the bottom water temperature at that location does not exceed 18[degrees]C or 19[degrees]C.

Lobsters in LIS frequently move to deeper water when shallower waters become too warm in summer months (Stewart 1972). In 1999, nearshore water temperatures in western LIS probably induced the hyperabundant lobsters to further concentrate in deep water in the summer and early autumn. Lobster displacement from shallow waters was noted by lobstermen fishing in central and western LIS (Crismale 2000, Doll 2000).

These warm water conditions may also have accelerated the growth of natural populations of the parasitic paramoeba, identified as Neoparamoeba pemaquidensis, found infecting the lobsters in 1999 (Mullen et al. 2005). In late October, more than 90% of lobsters examined were infected with paramoebae; those collected later in the fall had infection rates of about 29% (P. Howell, CTDEP, pers. comm.). This paramoeba inhabited LIS prior to 1999 (Mullen et al. 2005), therefore, it is possible that paramoebiasis was beginning to infect the lobster population prior to 1999. Unfortunately none of the lobsters that died in 1997 or 1998 was set aside for a pathologic work-up. Strains of N. pemaquidensis are facultative pathogens of sea urchins (affecting the nerve ring), salmon and, now, American lobsters (Mullen et al. 2005). The presence of paramoebae in lobsters was monitored for 3 years following the 1999 die-off; more than 800 lobsters collected systematically throughout the Sound by CTDEP and examined by pathologists at the University of Connecticut exhibited infection rates of 0% to 14% (P. Howell, CTDEP, pers. comm.)

Oxygen-depleted Waters

Since the late 1980s, the CTDEP Water Management Bureau has monitored water quality throughout the Sound. Dissolved oxygen data are used to assess the severity and extent of hypoxic conditions that develop in late summer in western LIS, which in 1999 were not especially severe (Gates 2000). Hypoxic conditions were present from July 2nd through August 21st, covering about 120 sq. miles (http://dep.state.ct.us/wtr/lis/monitoring/ summer99.htm). Hypoxic conditions were most severe during the first week of August. Data also showed a strong correlation between elevated bottom water temperatures and low bottom water dissolved oxygen levels in a west-to-east gradient across the Sound.

Three years of survey work by CTDEP in the early 1990s produced a response curve for lobsters with respect to hypoxic areas. Lobsters were found to "herd" or crowd in greater numbers near margins of hypoxic zones where dissolved oxygen (DO) concentrations were >2 mg/L, and leave areas where DO was [less than or equal to]2 mg/L (Simpson 2000). This suggests that as the lobsters moved from shallow to deeper waters to find cooler water in summer 1999, they were at the same time avoiding severely hypoxic areas, with the result that the lobster population was further concentrated in certain regions of western LIS.

Hostile Sediments

During the summer, hypoxia is a "top down" event in near bottom waters. Eutrophic conditions trigger algal blooms leading to subsequent high biological oxygen demand as the phytoplankton die and sink. However, in the spring and fall, hypoxia in bottom waters (sediment-water interface or nephaloid layer) is a "bottom up" phenomenon (Cuomo et al. 2005). Even after the summer hypoxic event dissipates and the water column remixes, hypoxic conditions remain at the sediment-water interface. As organic material decays here, sulfides and ammonia are released from the sediments, creating adverse conditions in this very narrow benthic zone; these conditions are exacerbated by warm bottom water temperatures (Cuomo et al. 2005). Lobsters require more oxygen as water temperature increases, which is unavailable in hypoxic waters.

Laboratory experiments demonstrated that lobsters exposed to the combined effects of ammonia, sulfides and low dissolved oxygen were increasingly susceptible to microbial infection from the pathogen, Aerococcus viridans, at normal summer temperatures (Robohm et al. 2005). Additional experiments showed that whereas high water temperature (24[degrees]C) had no lethal effect on disease-free eastern LIS lobsters as long as dissolved oxygen was kept high, low dissolved oxygen at 24[degrees]C killed 90% of the lobsters in 8 days (Draxler et al. 2005). Exposure to varying concentrations of sulfides and ammonia significantly increased the mortality rate at high water temperature and low dissolved oxygen (Draxler et al. 2005).

In August 1999, the temperature differential between surface and bottom water temperatures in LIS was as much as 5[degrees]C and both nearshore waters and deep bottom waters continued to warm (CTDEP 1999, Wilson & Swanson 2005). On August 29th, the effects of Hurricane Dennis to the south of LIS, coupled with strong winds associated with a fast moving cold front from the north that passed through the LIS region, caused a complete vertical mixing of the water column, raising bottom water temperature several degrees to >22[degrees]C (Wilson et al. 2004, Wilson & Swanson 2005).

Following the passage of this front, there was, according to temperature and salinity data, limited restratification until September 16th, when Tropical Storm Floyd passed through the region, resulting in a substantial rainfall event and causing additional mixing of the water column. Water monitoring data for August through October indicate that bottom water temperatures remained elevated above 20[degrees]C (CTDEP 1999), a condition which Powers et al. (2004), Chang (2004), and Draxler et al. (2005) report induces respiratory stress in lobsters.

Pesticides

Laboratory studies demonstrated that the pesticides malathion, resmethrin and methoprene are immunotoxic in lobsters, and that sublethal pesticide-related changes to the immune systems of lobsters can occur at certain exposure levels (De Guise et al. 2004a, 2004b, De Guise et al. 2005, Walker et al. 2005, Zulkosky et al. 2005). Significant sublethal effects on all life stages of lobsters were reported from the laboratory research, with resmethrin being most toxic, followed by malathion and methoprene (De Guise et al. 2004a, 2004b, De Guise et al. 2005, Walker et al. 2005, Zulkosky et al. 2005). (3)

The results of the two independent modeling exercises indicate that concentrations of individual pesticides in the water column of the western LIS basin could not have been high enough to cause adult lobster mortality throughout LIS in 1999, even considering the "worst case" parameters assuming 100% run-off (Miller et al. 2005, Wilson et al. 2005). The Phase I run for methoprene showed that even if all of the pesticide applied reached the water and never decayed, the concentration would not have been lethal to either larval or adult lobsters (Miller 2004, Miller et al. 2005). The LC50 level determined for adult lobsters exposed to resmethrin was 4 (Phase I) to 30 times (Phase II) higher than the maximum concentration of resmethrin modeled (Miller 2004, Miller et al. 2005). The LC50 for adult lobsters exposed to malathion was 24 times greater than the maximum concentration of malathion calculated in the bottom waters (Miller 2004, Miller et al. 2005). Wilson et al. (2005) modeled concentrations of malathion, resmethrin, and sumithrin following the "Phase II" scenario (which assumes all of the pesticide applied reaches the water column and then undergoes decay) and determined that there was little evidence that bottom concentrations exceeded 0.001 ppb within the interior of the western LIS basin for any of the three pesticides modeled.

The lobster industry's legal counsel contracted a third modeling effort to look at pesticide concentrations. While the results were comparable to those of the other two modeling exercises (maximum modeled concentrations smaller than LC50 concentrations), the lobster industry has raised further questions regarding the pesticide loadings and how they were incorporated into the SCLDR-supported modeling efforts (J. O'Donnell, University of Connecticut, pets. comm., N. Crismale & J. Finke, pers. comm.). The SCLDR is considering supporting additional modeling runs to address some of these concerns.

"A Perfect Storm" Leads to Lobster Mortality

There is overwhelming evidence that in the absence of any pesticide application, a confluence and succession of factors pushed the balance of the WLIS lobster population far out of equilibrium with its environment in 1999. Faced with disease, and subjected to sustained and increasingly hostile environmental conditions, the immune systems of the lobsters were unable to compensate, and many lobsters succumbed. While the main mortality event occurred in 1999, the problem may have been building for several prior years. There is no way to know now when the lobsters first began to be infected with paramoebae, or whether the inhospitable environmental conditions and an unusually large abundance of lobsters led to the infection, or simply exacerbated an infection already smoldering amid the lobster population.

Crowded conditions can increase the susceptibility of animals to disease, and its spread among a population (S. Frasca, University of Connecticut, pers. comm.). So far, scientists have been unable to fulfill Koch's postulates by culturing the paramoeba and infecting healthy lobsters with paramoebiasis; there is still much to be learned about this disease and its transmission. It is also important to note that populations of other crustaceans and some echinoderms also suffered some degree of mortality in 1999. However, none were examined, and so it can never be known if paramoebiasis played a role in mortalities of these taxa.

Sustained, above average water temperature was a driving force behind the snowball effect of environmental and oceanographic factors that stressed lobsters to the point at which their physiology and immune systems could not cope with these sustained and increasingly lethal environmental conditions in conjunction with, or in addition to, mounting an immune defense against the parasitic amoebae. Based on the body of evidence, the scenario leading to the 1999 mortality event is proposed as follows:

* Scattered reports of atypical lobster mortality began as early as 1997, however it is unknown when paramoebiasis began to affect the lobster population.

* In 1999, water temperature remained several degrees warmer than average for a duration of many months. For much of the summer and continuing into early fall, bottom water temperature remained at or above the temperature threshold that, in lobsters, induces a significantly enhanced respiration rate. The warm waters also likely accelerated the growth of natural populations of Neoparamoeba pemaquidensis in LIS waters.

* Lobsters in western LIS concentrated in numbers as they moved to deeper waters to escape warm shallower waters and moved away from hypoxia-affected areas towards those with slightly higher DO concentrations. This displacement, exacerbated by the abundant lobster population, caused crowding that, in the presence of less-than-optimal conditions, increased susceptibility to disease.

* In late August, winds from a front moving through the region completely mixed the water column in matter of hours, brought warm surface waters to the bottom, and raised warm temperatures several more degrees. While lobsters typically can endure abrupt changes in temperature, these lobsters were already in a weakened physiological state.

* Pesticides were being applied to combat the spread of WNV by mosquitos. Exposure of some lobsters in near-coastal waters to these pesticides could have resulted in sublethal effects, which may have further weakened those lobsters.

* As summer hypoxic conditions dissipated, low DO at the watersediment interface coupled with high water temperatures facilitated the release of sulfides and ammonium from the sediments, conditions shown to lead to a significant increase in the rate of mortality.

* Affliction with paramoebiasis sealed the fate of these lobsters. Either the energy used in mounting a sustained immune response to the disease took its toll on the lobsters, or the lobsters were unable to mount an adequate response as their immune systems were potentially compromised by the stressful conditions presented by this "perfect storm" of lethal synergistic effects. Mortality became rampant and the commercial lobster fishery in western LIS largely collapsed.

Much of the cause of the mortality event was surmised during the April 2000 symposium, but not all of the pieces of the puzzle were evident in an empirical sense, nor was it clear how they fit together. Commercial landings have demonstrated that the harvestable resource in LIS declined significantly in 1999. Survey data also show sublegal lobsters died. Judging by the larval index, it seems that all life stages of lobsters were affected, underscoring a continued decline in landings, which now resemble average landings from the early 1980s (CTDEP & NYSDEC, pers. comms.). At no time since 1999 have lobster landings dropped to zero in LIS, however, landings (and concomitant fishing effort) have progressively declined in both central and eastern LIS. The 1999 event was not the first time that key marine resources in LIS have suffered declines; there have been other temporary declines of LIS commercial fisheries, including lobstering, in the 1950s and 1970s. Perhaps significantly, water temperature was elevated during those periods as well.

CONCLUSION

Time will tell if the LIS lobster population will rebound. Even in the absence of further disease outbreaks, equilibrium may ultimately shift geographically in the face of apparent localized warming trends. Lobsters in Long Island Sound, already at the distal southern extent of their inshore distribution, may be confronted with a range contraction due to long-term, unfavorable environmental conditions. Nonetheless, CTDEP, NYSDEC, ASMFC and the lobster industry are currently focusing their attention on identifying and implementing appropriate measures to protect and enhance the population of lobsters that remains in Long Island Sound, and thus work towards a sustainable commercial fishery.

The collective research efforts of the 3-year LIS Lobster Research Initiative have yielded extensive new information on (1) the interactions of American lobsters with their environment; (2) the physiological responses they express in the presence of individual and combinations of stressors; (3) new "tools" that now exist to examine immunological effects and (4) two new infectious lobster diseases (paramoebiasis and epizootic shell disease). The results greatly enhance the existing knowledge of American lobsters and provide information beneficial to researchers and resource managers throughout the range of this species.

ACKNOWLEDGMENTS

The work reported on in this article was supported by the National Oceanic and Atmospheric Administration (NOAA) National Marine Fisheries Service; the Connecticut Sea Grant College Program, NOAA Award No. NAI6RG1364; the New York Sea Grant Institute, NOAA Award No. NA16RG1354; the State of Connecticut through the Connecticut Department of Environmental Protection, Office of Long Island Sound Programs and the US Environmental Protection Agency, Long Island Sound National Estuary Program. The views expressed are those of the authors and do not necessarily represent those of the funding agencies or members of the Steering Committtee for Lobster Disease Research.

LITERATURE CITED

Aiken, D. E. & S. L. Waddy. 1986. Environmental influences on recruitment of American lobsters (Homarus americanus): a perspective. Can. J. Fish. Aquat. Sci. 43(11):2258-2270.

Balcom, N. (Ed.). 2000. Summary of research priorities for the Long Island Sound lobster resource. First Long Island Sound Lobster Health Symposium, April 17-18. Stamford, CT. 8 pp.

Balcom, N. (Ed.). 2003. Summary of presentations of the Third Long Island Sound Lobster Health Symposium. March 7, Bridgeport, CT: Connecticut Sea Grant No. CT-SG-03-03. 13 pp.

Chang, E. 2004. Stress indicators in crustaceans: crustacean hyperglycemic hormone and stress proteins. Presentation at second working meeting of LIS Lobster Research Initiative. May 3-4, Groton, CT.

Cobb, S. J. 1976. The American lobster: the biology of Homarus americanus. Rhode Island Sea Grant Marine Tech. Rpt. No. 49. 32 pp.

Cooper, R. A. & J. R. Uzmann. 1980. Ecology of juvenile and adult Homarus. In: J. S. Cobb, & B. F. Phillips, eds. The biology and management of lobsters. Vol. II. Ecology and management. New York: Academic Press. pp. 97-142.

CTDEP. 2000. Impact of 1999 lobster mortalities in Long Island Sound. Connecticut Department of Environmental Protection, Marine Fisheries Office, Old Lyme, CT. 46 pp plus appendices.

CTDEP. 1999. Monitoring data summaries from Long Island Sound water quality monitoring program survey. State of Connecticut Department of Environmental Protection.

Cuomo, C., R. Valente & D. Dogru. 2005. Seasonal variations in sediment and bottom water chemistry of western Long Island Sound: implications for lobster mortality. J. Shellfish Res. 24(3):805-814.

Cuomo, C., D. Dogru, R. Valente, A. F. J. Draxler, A. Deshpande, J. Howard, D. Wieczorek, D. Kapareiko, R. Robohm, R. Sherrell, J. C. Varekamp, E. Thomas, M. Buchholtz ten Brink, M. Altabet, S. Cooper, F. Sangiorgi, R. Wilson, R. L. Swanson, D. Waliser, G. Lopez, & R. Cerrato. 2004. The role of physical/chemical conditions in lobster mortality in Long Island Sound. Presentation at Fourth Long Island Sound Lobster Health Symposium, October 4, Stony Brook, NY.

DeFur, P., S. Burr, N. Crismale,, G. Doll, J. Finke, R. Frate, R. French, M. Gates, J. Makowsky & D. Simpson, 2000. Transcripts, First Long Island Sound Lobster Health Symposium, April, 16-17, unpublished. Stamford, CT: Connecticut Sea Grant College Program. 196 pp.

De Guise, S., J. Maratea, E. S. Chang & C. Perkins. 2005. Resmethrin immunotoxicity and endocrine disrupting effects in the American lobster (Homarus americanus) upon experimental exposure. J. Shellfish Res. 24(3):781-786.

De Guise, S., J. Maratea & C. Perkins. 2004a. Malathion immunotoxicity in the American lobster (Homarus americanus) upon experimental exposure. Aquat. Toxicol. 166:419-425.

De Guise, S., A. McElroy, B. Brownawell, M. Horst, E. Chang & C. Perkins. 2004b. The role of pesticides in the Long Island Sound lobster die-off. Presentation at Fourth Long Island Sound Lobster Health Symposium. October 4, Stony Brook, NY.

Dove, A. D. M., B. Allam, J. J. Powers & M. S. Sokolowski. 2005. A prolonged thermal stress experiment on the American lobster, Homarus americanus. J. Shellfish Res. 24(3):761-765.

Dove, A., B. Allam, R. Anderson, R. Cerrato, E. S. Chang, A. F. J. Draxler, J. Factor, H. Laufer, G. Lopez & R. Robohm. 2004. Physiological responses to stress. Presentation at Fourth Long Island Sound Lobster Health Symposium. October, 4 Stony Brook, NY

Draxler, A. F. J., R. A. Robohm, D. Wieczorek, D. Kapareiko & S. Pitchford. 2005. Effect of habitat biogeochemicals on survival of lobsters (Homarus americanus). J. Shellfish Res. 24(3):821-824.

Frasca, S., A. Chistoserdov, R. Smolowitz, A. Hsu, K. Nevis, T. Mullen, P. Gillevet, C. O'Kelly, M. Peglar, T. Nerad & R. Gast. 2004. Parasites and diseases. Presentation at Fourth Long Island Sound Lobster Health Symposium, October 4. Stony Brook, NY.

French, R. 2000a. Transcripts, First Long Island Sound Lobster Health Symposium, 16-17 April, Stamford, CT. Unpublished. Connecticut Sea Grant College Program, 196 pp.

French, R. 2000b. LIS lobster morbidity and mortality, 1999-2000. Pathology report from the University of Connecticut, Department of Pathobiology and Veterinary Services, September 28.7 pp.

Herrick, F. H. 1911. Natural history of the American lobster. Bull. U.S. Bur. Fish. 29(1909): 149-408.

Howell, P., J. Benway, C. Giannini, K. McKown, R. Burgess & J. Hayden. 2005. Long-term population trends in American lobster (Homarus americanus) and their relation to temperature in Long Island Sound. J. Shellfish Res. 24(3):849-857.

Kinne, O. 1970. Temperature: animals-invertebrates. In: O. Kinne, editor. Marine ecology. Volume 1. Environmental factors, Part 1. London: Wiley Interscience. pp. 407-514.

Lawton, P. & K. L. Lavalli. 1995. Postlarval, juvenile, adolescent, and adult ecology. In: J. R. Factor, editor. Biology of the lobster, Homarus americanus. New York: Academic Press. pp. 47-88.

LoBue, C., J. Hayden, P. LoCicero, R. Burgess, P. Howell, K. Gottschall & C. Giannini. 2003. Fishery-dependent monitoring of Long Island Sound lobsters. Presentation at Third Long Island Sound Lobster Health Symposium, March 7, Bridgeport, CT.

McKown, K., R. Burgess, J. Hayden, P. Howell, C. Giannini & J. Benway. 2004. Long-term lobster population trends in Long Island Sound. Presentation at Fourth Long island Sound Lobster Health Symposium, 4 October, Stony Brook, NY.

McLeese, D. W. 1956. Effects of temperature, salinity, and oxygen on the survival of the American lobster. J. Fish. Res. Board Can. 13(2):247-272.

Mercaldo-Allen, R. & C. A. Kuropat. 1994. Review of American lobster (Homarus americanus) habitat requirements and responses to contaminant exposures. NOAA Technical Memorandum NMFS-NE-105, NOAA, NMFS, Dept. of Commerce. 52 pp.

Miller, R. L., J. R. Wands, K. N. Chytalo & R. A. D'Amico. 2005. Application of water quality modeling technology to investigate the mortality of lobsters (Homarus americanus) in Western Long Island Sound during the summer of 1999. J. Shellfish Res. 24(3):859-864.

Miller, R. L. 2004. Applying water quality modeling to investigate the summer of 1999 decline in Long Island Sound lobsters. Presentation at Fourth Long Island Sound Lobster Health Symposium. October 4, Stony Brook, NY.

Mullen, T. E., K. R. Nevis, C. J. O'Kelly, R. J. Gast & S. Frasca, Jr. 2005. Nuclear small-subunit ribosomal RNA gene-based characterization, molecular phylogeny, and PCR detection of the Neoparamoeba from western Long Island Sound Lobster. J. Shellfish Res. 24(3):719-731.

Pearce, J. 2004. The 1999 lobster mortality event-fitting together pieces of the puzzle. Presentation at Fourth Long Island Sound Lobster Health Symposium. October 4, Stony Brook, NY.

Powers, J., G. Lopez, R. Cerrato & A. Dove. 2004. Effects of thermal stress on Long Island Sound Lobsters, H. americanus. Presentation during second working meeting of LIS Lobster Research Initiative. May 3-4, Groton, CT.

Prosser, C. L. 1973. Comparative animal physiology, 3rd ed. Philadelphia: Saunders. 966 pp.

Robohm, R. A., A. F. J. Draxler, D. Wieczorek, D. Kapareiko & S. Pitchford. 2005. Effects of environmental stressors on disease susceptibility in American lobsters: a controlled laboratory study. J. Shellfish Res. 24(3):773-779.

Stewart, L. L. 1972. The seasonal movement, population dynamics, and ecology of the lobster, Homarus americanus (Milne-Edwards) off Ram Island, Connecticut. Ph.D. dissertation, University of Connecticut. 112 pp.

US Department of Commerce. 2000. Commerce Secretary Daley announces lobster fishery failure in Long Island Sound. Press release. January 26. 2 pp.

Varekamp, J., E. Thomas. M. Buchholtz ten Brink, M. Altabet, S. Cooper & F. Sangiorgi. 2004. Environmental change in Long Island Sound in the recent past: eutrophication and climate change. Presentation at second working meeting of LIS Lobster Research Initiative. May, 3-4 Groton, CT.

Walker, A. N., P. Bush, T. Wilson, E. Chang, T. Miller & M. N. Horst. 2005. Metabolic effects of acute exposure to methoprene in the American lobster, Homarus americanus. J. Shellfish Res. 24(3):787-794.

Wilson, R. E., H. Crowley, B. Brownawell & R. L. Swanson. 2005. Simulations of transient pesticide concentrations in Long Island Sound for late summer 1999 with a high resolution coastal circulation model. J. Shellfish Res. 24(3):865-875.

Wilson, R. E. & R. L. Swanson. 2005. A perspective on bottom water temperature anomalies in Long Island Sound during the 1999 lobster mortality event. J. Shellfish Res. 24(3):825-830.

Wilson, R., R. L. Swanson & D. Waliser. 2004. Summary points concerning prevailing water conditions. Presentation at second working meeting of LIS Lobster Research Initiative. May 3-4, Groton, CT.

Zulkosky, A. M., J. P. Ruggieri, S. A. Terracciano, B. J. Brownawell & A. E. McElroy. 2005. Acute toxicity of resmethrin, malathion, and methoprene to larval and juvenile American lobsters (Homarus americanus) and analysis of pesticide levels in surface waters after Scourge[TM], Anvil[TM], and Altosid[TM] application. J. Shellfish Res. 24(3):795-804.

(1) It should be noted that many lobstermen from CT and NY, including the SCLDR industry members, dispute the conclusions presented at the October 2004 symposium, singling out pesticides used for mosquito control as the only factor that was new or different in 1999. They are represented in a class action civil lawsuit filed against the manufacturers of the pesticides.

(2) A "stress degree day" was calculated as the number of days per year when the bottom water temperature at a station in the Sound exceeded 20[degrees]C, taking into account the degree to which it was over 20[degrees]C. For example, if for one day the temperature was 22[degrees]C, then that would be equal to two stress degree days.

(3) The effect of sumithrin on American lobsters was not determined as part of this research initiative because it was not proposed for consideration in any of the studies.

JACK PEARCE (1) AND NANCY BALCOM (2) *

(1) NOAA Fisheries (retired); Marine Pollution Bulletin," Buzzards Bay Laboratory, 54 Upland Road, Falmouth, Massachusetts 02540; (2) Connecticut Sea Grant College Program, University of Connecticut, 1080 Shennecossett Road, Groton, Connecticut 06340

* Corresponding author. E-mail: [e-mail]