STRANGFORD LOUGH ECOLOGICAL CHANGE INVESTIGATION (SLECI)

Transcription

1 STRANGFORD LOUGH ECOLOGICAL CHANGE INVESTIGATION (SLECI) Work Package 9. Harmful Algal Blooms, Diseases and Parasites 9.1 TOXIN PRODUCING AND NUISANCE MICROALGAE IN STRANGFORD LOUGH, NORTHERN IRELAND: AN OVERVIEW FROM 1996 TO Prepared by School of Biology and Biochemistry Queen s University Belfast Belfast BT9 7BL Northern Ireland June 2004 Prepared for Environment and Heritage Service Department of the Environment Commonwealth House Belfast BT1 1GU Northern Ireland Recommended citation: Roberts, D., Davies, C., Mitchell, A., Moore, H., Picton, B., Portig, A., Preston, J., Service, M., Smyth, D., Strong, D. and Vize, S. (2004). Strangford Lough Ecological Change Investigation (SLECI). Report to Environment and Heritage Service by the Queen s University, Belfast. The opinions expressed in this report do not necessarily reflect the current opinion or policy of Environment and Heritage Service

2 Contents 1 Introduction Methods Results Non-toxic algal blooms in Strangford Lough, Northern Ireland Discussion References...9 Strangford Lough Ecological Change Investigation [SLECI] i

3 1 Introduction An algal bloom is typically a rapid population increase, indicating an abundance of nutrients and ideal growing conditions, although population increases can also occur due to hydrographic concentration or a lack of topdown control, i.e. reduced grazing. Generally, these are naturally occurring events, although there is an apparent increase in their frequency and distribution worldwide: this has been attributed to coastal zone management, eutrophication, non-native introductions and increasing scientific awareness (Hallegraeff et al., 2003). Microalgal blooms are often striking events causing discolouration of the water i.e. a red tide and/or excessive accumulations of sea foam or unpleasant odour. Although many marine algal blooms that discolour the water are harmless, some species can produce toxins potentially harmful to humans and/or marine life, e.g. Alexandrium spp. and Dinophysis spp. Shellfish for human consumption are monitored for toxins under the requirements of the EC Shellfish Hygiene Directive. Council Directive 91/492/EEC requires member states to monitor shellfish harvesting areas for toxin-producing microalgae: both water samples and shellfish flesh are examined. The competent authority for the sampling programme is the Food Standards Agency, who arranges the collection and delivery of the water samples to a local laboratory, in the case of Northern Ireland this is the Aquatic Systems Group at DARDNI (Department of Agriculture and Rural Development, Northern Ireland). 2 Methods Four sites, namely Marlfield Bay, Paddy s Point, Reagh Bay and Skate Rock (Figure 1), have been consistently sampled in Strangford Lough from 1996 to Mount Stewart and Castle Espie have only been sampled in 2002 and Fieldwork was undertaken as close to high tide as possible and a one litre water sample collected with an integrated tube sampler approximately 1-2 metres below the surface. All samples were preserved using acidified Lugol s iodine solution. A 50 ml -1 subsample was taken from the integrated sample this gives a detection limit of 20 cells L -1. This subsample was allowed to settle overnight before being examined using an inverted microscope. There are 21 target species; their associated toxin and threshold density values are shown in Table 1. Strangford Lough Ecological Change Investigation [SLECI] 1

4 Figure 1. Sites within Strangford Lough monitored since 1996 for toxin producing and nuisance microalgae. Blue dot is Skate Rock ( N W); Yellow dot is Marlfield Bay ( N W); Green dot is Reagh Bay ( N W); a red box surrounds Paddy s Point ( N W. Table 1. Monitored microalgae in Strangford Lough, Northern Ireland. Species Toxin/Effects Threshold value Alexandrium minutum Paralytic shellfish toxin Presence Alexandrium tamarense Paralytic shellfish toxin Presence Chrysochromulina polylepis Toxic to fish None Dinophysis acuminata Diarrheic shellfish toxin > 100 cells L -1 Dinophysis acuta Diarrheic shellfish toxin > 100 cells L -1 Dinophysis norvegica Diarrheic shellfish toxin > 100 cells L -1 Dinophysis rotundata Diarrheic shellfish toxin > 100 cells L -1 Dictyocha speculum Harmful to fish None Gymnodinium mikimotoi Toxic to fish None Gymnodinium catenatum Paralytic shellfish toxin Presence Gymnodinium spp. Some species toxic to fish None Heterosigma akashiwo Toxic to fish None Lingulodinium polyedrum Yessotoxin (DSP like) > 100 cells L -1 Noctiluca scintillans Toxic to fish None Prorocentrum lima Diarrheic shellfish toxin > 100 cells L -1 Prorocentrum minimum Venerupin shellfish poisoning None Pseudo-nitzschia spp. Amnesic shellfish poisoning > 150,000 cells L -1 Prymnesium parvum Toxic to fish None Phaeocystis sp. Not known None Protoperidinium spp. DSP like Presence Strangford Lough Ecological Change Investigation [SLECI] 2

5 3 Results Of the 21 target species in Table 1, 14 species were found in Strangford Lough. Those not detected included Alexandrium minutum, Chrysochromulina polylepis, Gymnodinium catenatum, Heterosigma akashiwo, Lingulodinium polyedrum and Prymnesium parvum. Dinophysis rotundata and Noctiluca scintillans occurred at very low concentrations and did not exceed more than 60 cells per litre during the survey period. Low cell concentrations were also found for Alexandrium tamarense (max. 180 cells L -1 ), Dinophysis acuminata (max. 400 cells L -1 ), Dinophysis acuta (max. 480 cells L -1 ), Gymnodinium mikimotoi (max. 520 cells L -1 ), Protoperidinium spp (max. 540 cells L -1 ) and Prorocentrum lima (max. 800 cells L -1 )(Mount Stewart 2003 only). The following species occasionally occurred at concentrations greater than 1000 cells per litre: Dinophysis norvegica (Figure 2), Dictyocha speculum (Figure 3), Gymnodinium spp. (Figure 4), Pseudo-nitzschia spp. (Figure 5) and Phaeocystis sp. (Figure 6). Prorocentrum lima typically occurred at low cell concentrations, i.e. less than 100 cells per litre at both Mount Stewart and Castle Espie. However, this species increased in cell concentration to 3,520 cells per litre in April 2002 in Mount Stewart Bay (only data for 2001 and 2002 are available). Only during July 1996 and to a lesser extent July 2001 was Dinophysis norvegica (Figure 2) present in any real quantity during the seven year period. In Marlfield Bay, the cell count approached 1,100 cells per litre during July 1996 and approximately 500 cells per litre at Skate rock at the same time. The second peak in abundance in 2001, also at Marlfield Bay and Skate Rock, was only a fifth of that seen in The cell concentration of Dictyocha speculum at four sites in Strangford Lough appears to have little periodicity, although most of the peaks in abundance appear to occur in September (Figure 3). Typically, cell numbers did not exceed 400 per litre, although high abundance events were apparent in 1997 and 2003 with concentrations greater than 1,000 cells per litre. The largest of these peaks occurred late in 2003 with cell counts at Reagh Bay and Paddy s Point approaching 1,500 cells per litre. Gymnodinium spp. rarely exceeded 400 cells per litre at any of the four sites. The only exception to this was in May 2000 when cell counts rose to over 8,500 at Paddy s Point and over 2,000 cells per litre at Reagh Bay (Figure 4). The cell abundance of Pseudo-nitzschia spp. peaked consistently in May each year at all sites with cell counts exceeding 80,000 (Figure 5). The greatest abundance happened in 1999 when the cell concentration exceeded 128,000. The abundance of this species varied greatly between the four sites with no one site being consistently higher between years. Strangford Lough Ecological Change Investigation [SLECI] 3

6 Peaks in the abundance of Phaeocystis sp. occurred irregularly throughout the summer months and between the four sites (Figure 6). Most of the peaks in cell concentration were usually much less than 4,000 cells per litre. However, in September 2001 and April 2002 Phaeocystis sp. peaked at 14,000 cells per litre. A lesser peak of abundance occurred in May 2003 when concentrations approached 9,000 cells per litre Cells per litre Marlfield Bay Paddy's Point Reagh Bay Skate Rock /01/96 22/07/96 22/01/97 22/07/97 22/01/98 22/07/98 22/01/99 22/07/99 22/01/00 22/07/00 22/01/01 22/07/01 22/01/02 22/07/02 22/01/03 22/07/03 Figure 2. Cell concentration of Dinophysis norvegica at four sites in Strangford Lough ( ) Cells per litre /01/96 22/07/96 22/01/97 22/07/97 22/01/98 22/07/98 22/01/99 22/07/99 22/01/00 22/07/00 22/01/01 22/07/01 22/01/02 22/07/02 22/01/03 22/07/03 Marlfield Bay Paddy's Point Reagh Bay Skate Rock Figure 3. Cell concentration of Dictyocha speculum at four sites in Strangford Lough ( ). Strangford Lough Ecological Change Investigation [SLECI] 4

7 Cells per litre Marlfield Bay Paddy's Point Reagh Bay Skate Rock /01/96 22/07/96 22/01/97 22/07/97 22/01/98 22/07/98 22/01/99 22/07/99 22/01/00 22/07/00 22/01/01 22/07/01 22/01/02 22/07/02 22/01/03 22/07/03 Figure 4. Cell concentration of Gymnodinium spp. at four sites in Strangford Lough ( ) Cells per litre /01/96 22/07/96 22/01/97 22/07/97 22/01/98 22/07/98 22/01/99 22/07/99 22/01/00 22/07/00 22/01/01 22/07/01 22/01/02 22/07/02 22/01/03 22/07/03 Marlfield Bay Paddy's Point Reagh Bay Skate Rock Figure 5. Cell concentration of Pseudo-nitzschia spp. at four sites in Strangford Lough ( ). Strangford Lough Ecological Change Investigation [SLECI] 5

8 Cells per litre Marlfield Bay Paddy's Point Reagh Bay Skate Rock 0 22/01/96 22/07/96 22/01/97 22/07/97 22/01/98 22/07/98 22/01/99 22/07/99 22/01/00 22/07/00 22/01/01 22/07/01 22/01/02 22/07/02 22/01/03 22/07/03 Figure 6. Cell concentration of Phaeocystis sp. at four sites in Strangford Lough ( ). 3.1 Non-toxic algal blooms in Strangford Lough, Northern Ireland Table 2 shows the date, species and location of some of the non-toxic algal blooms at sites monitored for toxic algal in Strangford Lough. Typically, only the toxic species are enumerated, but when a noteworthy bloom of a nontoxic species has occurred, a note has been made. No cells counts have been made of these non-toxic species and only the sites used for regular shellfish collections were monitored and this is only when for bloom activity. Table 2. Non-toxic algal blooms in Strangford Lough, Northern Ireland. Year Date Species Location No records /04/02 Eutreptiella sp. Castle Espie 08/07/02 Eutreptiella sp. Mount Stewart /09/01 Eutreptiella sp Mount Stewart /08/00 Asterionellopsis glacialis Reagh Bay and Paddy's Point /06/97 Unidentified microflagellate Reagh Bay 21/07/97 Eutreptiella sp. Reagh Bay and Paddy's Point /05/96 Chaetoceros sp. Reagh Bay and Paddy's Point 13/06/96 Unidentified microflagellate Strangford Bay 06/08/96 Chaetoceros socialis Reagh Bay and Paddy's Point /06/95 Unidentified microflagellate Strangford Bay Strangford Lough Ecological Change Investigation [SLECI] 6

9 4 Discussion Noteworthy peaks of abundance include: April 2002, Prorocentrum lima in Mount Stewart Bay. July 1996, Dinophysis norvegica at Marlfield Bay and 2003, Dictyocha speculum at Reagh Bay and Paddy s Point. May 2000, Gymnodinium spp. at Paddy s Point and at Reagh Bay. May 1997, 1998, 1999 and 2003 for Pseudo-nitzschia spp. at all four sites. September 2001 and April 2002, Phaeocystis sp. at Paddy s Point. The objective of this review is to assess the potential impact of toxic algae on the ecology of Strangford Lough rather than the health implications for humans. Therefore, the thresholds detailed in Table 1 provide no real guide about the levels of toxicity posed and resulting ecological impact. Other studies have examined the effect of toxic algal blooms on benthic assemblages. Simon and Dauer (1977) documented the mass invertebrate die-off in Tampa Bay (Florida) following a bloom of Gymnodinium breve. The mortalities were not caused directly by toxic effect of the bloom, but resulted from anaerobic conditions created along a small area of intertidal associated with the natural deposition and subsequent decomposition of dead fish that had been killed directly by toxins (Simon and Dauer 1972). Conversely, the mass biotic die-off in Wellington Harbour (New Zealand), reported by Wear and Gardner (2001), resulted directly from the amount of toxin produced by a bloom of Karenia brevisulcata. This resulted in substantial mortalities of polychaetes, gastropods, bivalve molluscs, echinoderms, decapod crustaceans and fish associated with the substratum. At Wellington Harbour, the cell concentration of Karenia brevisulcata reached a peak of over 33 x 10 6 cells per litre before the toxin was concentrated enough to induce the die-off. Even after allowing for a substantial variation in the differing toxicity between microalgal species, the cell concentrations in Strangford Lough were several orders of magnitude lower than that observed in Wellington Harbour, which makes the probability of toxin-induced benthic mortalities highly unlikely. This is further supported by the findings of Matsuyama et al. (2000) who examined the survival of Pacific oyster larvae in differing bloom conditions, i.e. species and concentrations. Even at cell concentrations of 1 x10 6 for Gymnodinium catenatum and G. mikimotoi, there was no detectable increase in larval mortality. The organic biomass required to generate hypoxic conditions in Tampa Bay was great and appeared to be supplied by a massive fish die-off. In Table 1, many of the microalgal species listed are toxic to fish, although no thresholds are provided. The poisoning of fish and resulting hypoxic conditions does provide a possible route for toxic blooms to impact on the benthic habitats in Strangford Lough. Furthermore, Dictyocha speculum and Gymnodinium spp. were both recorded in Strangford Lough and are known to be toxic to fish. Despite the presence of this pathway from microalgal bloom to benthic Strangford Lough Ecological Change Investigation [SLECI] 7

10 impact, no information exists that might help establish a probability for this event. Without known bloom thresholds for fish poisoning, it is impossible to establish whether this type of event has happened in Strangford Lough. One would suspect that large and widespread fish kills would be noticed by users of Strangford Lough none have been reported. Although the time and location of the non-toxic algal blooms have been recorded, they show a clear geographic sampling bias towards the areas routinely sampled. Equally, no cell counts were made during the blooms of the non-toxic species, making interpretation difficult. It is possible that nontoxic blooms could impact benthic habitats through the decomposition of excessive organic material and the resulting localized hypoxia. Whether this process occurs in Strangford Lough remains unknown and requires further investigation. To conclude, there is no evidence to suggest that toxic algal blooms are a problem in Strangford Lough or that they have impacted on benthic communities. Little is known about the extent of the non-toxic blooms in the Lough or their effects on the benthic habitats. Further research into the abundance and spatial scale of the blooms and the benthic enrichment caused would benefit their interpretation. Strangford Lough Ecological Change Investigation [SLECI] 8

11 5 References Hallegraeff G M, Anderson D M and Cembella A D Manual on harmful marine microalgae. Monographies on Oceanographic Methology. United Nations Educational, Scientific and Cultural Organization. pp, Matsuyama Y, Usuki H, Uchida T and Kotani Y Effects of harmful algae on the early planktonic larvae of the oyster Crassostrea gigas. IOC HAB Interactions between harmful microalgae and marine invertebrates 8: McCurdy G Monitoring of algal toxins in shellfish in Northern Ireland. Food Standards Agency Northern Ireland. McKinney, E.S.A Monitoring for toxin producing and nuisance microalgae in N. Ireland coastal waters. DARDNI report. McKinney, E.S.A Monitoring for toxin producing and nuisance microalgae in N. Ireland coastal waters. DARDNI report. McKinney, E.S.A Monitoring for toxin producing and nuisance microalgae in N. Ireland coastal waters. DARDNI report. Simon J. L. and Dauer D. M Reestablishment of a benthic community following natural defaunation. In Ecology of Marine Benthos. pp Ed. B. C. Coull. University of South Carolina Press, Wear R.G. and Gardner J.P.A Biological effects of the toxic algal blooms of February and March 1998 on the benthos of Wellington Harbour, New Zealand. Marine Ecology Progressive Series 281: Strangford Lough Ecological Change Investigation [SLECI] 9