Silver Gulls at Blackmans Bay Beach, Winter 2017

Water quality and the potential involvement of Silver Gulls at Blackmans Bay Beach, Winter 2017.

Report to Kingborough Council, October 2017 Dr Eric J Woehler, BirdLife Tasmania

Executive Summary

Unusually high numbers of Silver Gulls Chroicocephalus novaehollandiae were present on Blackmans Bay Beach during 2017, with flocks in excess of 2000 birds reported. Local residents expressed concerns to Kingborough Council regarding the potential adverse impacts on water quality and the volume of gull droppings on the beach over a period of several months.

Elevated levels of Enterococcus, a potential bacterial source of disease in humans were recorded in water samples from Blackmans Bay. A peak count of Enterococcus occurred following unusual and significant rainfall in December 2016, and another coincided with the presence of Silver Gulls at Blackmans Bay Beach, suggesting that alternative source(s) were likely responsible, rather than the Silver Gulls.

The absence of cloacal swabs from Silver Gulls prevents any testing or establishment of a causative link between the birds and high Enterococcus counts. At present, there are no data to support the proposal that the high Enterococcus counts recorded by Council and the DEP at Blackmans Bay Beach originated from the Silver Gulls present during 2017.

The cause(s) of the influx of the Silver Gulls to Blackmans Bay during 2017 cannot be determined at this time.

Silver Gulls at Blackmans Bay Beach, 11 August 2017. ©Eric J Woehler

BirdLife Tasmania Technical Report 2017 - 08

Written E Woehler PhD Reviewed V Ruoppolo DVM Submitted M Steele 24 October 2017

BirdLife Tasmania Technical Report 2017 – 08 Page 2 Context for this Study

BirdLife Tasmania was approached by Kingborough Council in August 2017, following numerous enquiries from members of the public who were concerned about the potential human health impacts associated with large (approximately 2000) flocks of Silver Gulls Chroicocephalus novaehollandiae present on the beach. BirdLife Tasmania was commissioned to prepare a report on the potential for human health issues arising from adverse impacts on water quality in the Derwent River and from the quantity of gull droppings on the beach. A meeting was held on site on 11 August 2017, with a subsequent visit on 17 September 2017; in both cases Silver Gulls were present, albeit fewer birds were present on the second visit.

This was the first time that many human residents of Blackmans Bay had observed gulls in high numbers present on a daily basis for an extended period (M Steele, Kingborough Council, pers. comm.). The numbers of Silver Gulls present on the beach increased from mid-February 2017 onwards. This contributed to community concerns regarding the potential for human health issues arising from what was perceived to be an “unusual” event.

1. Regional Silver Gull Population

The regional population of Silver Gulls (in addition to Kelp and Pacific Gulls) in southeast Tasmania has been monitored using a standardised annual count in June each year since 1983 (BirdLife Tasmania, unpublished data). In that time, the population has varied between fewer than 3000 individuals to more than 16,000 individuals. The regional populations of all three species of gulls are presently decreasing, with the regional Silver Gull population down 34% from its previous maximum in Winter 2014 (Figure 1).

Approximately 15 islands in southeast Tasmania are used for breeding by Silver Gulls (Figure 2). At least five islands in the d’Entrecasteaux Channel are used by Silver Gulls: Arch Rock, Green Island, Charity Island, Curlew Island and Little Southport Island. The estimated total breeding population for these islands is approximately 400 breeding pairs of Silver Gulls (BirdLife Tasmania, unpublished data).

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100 © BirdLife Tasmania % original datum

0 1980 1985 1990 1995 2000 2005 2010 2015 2020 Winter (mid-point 3Y running mean) Figure 1. Regional (southeast Tasmania) population data (expressed as 3-year running means) for Silver (red), Kelp (green) and Pacific Gulls (blue). No counts were undertaken 1990 to 1994 inclusive. Source: BirdLife Tasmania, unpublished data.

BirdLife Tasmania Technical Report 2017 – 08 Page 3 2. Silver Gull Breeding Season

In southeast Tasmania, the breeding season for Silver Gulls extends from approximately mid- to late- August until January, depending on the late-Winter and Spring weather conditions. Females lay 3 or 4 eggs over a 6 to 8 day period. Incubation of the eggs is approximately 3 weeks and the chicks fledge (leave the nest at 4 to 5 weeks of age, and fly at 6 – 7 weeks of age.

Within a colony, the eggs are laid over an extended period of 4 to 6 weeks, reflecting different arrival times of breeding birds to the colony. The species is highly asynchronous, resulting in the extended breeding season. Individual Silver Gull colonies in southeast Tasmania are deserted during February as adults and chicks leave the colonies and move to adjacent beaches and foreshores where the birds will forage and roost (rest) until the following breeding season.

Figure 2. Silver Gull breeding locations (base map from Brothers et al. 2001), with additional sites mapped based on BirdLife Tasmania surveys to 2015/16 (BirdLife Tasmania unpublished data).

3. Blackmans Bay Silver Gull Counts

Data from the annual Winter Gull Counts conducted by BirdLife Tasmania for Blackmans Bay Beach in toto are shown in Table 1. These counts are undertaken on the Sunday of the Queen’s Birthday long weekend in early- to mid-June annually, and counts of all species of gulls are obtained. The Blackmans Bay Beach counts cover the entire length of the beach.

For the period 2009 to 2016 inclusive (ie excluding 2017), the mean number of Silver Gulls recorded on

BirdLife Tasmania Technical Report 2017 – 08 Page 4 Blackmans Bay Beach in total was 43 ± 36 birds. Including the 2017 count (1000 birds), the mean is 150 ± 321 birds.

For the period 2009 to 2016 inclusive, the numbers of Silver Gulls present on Blackmans Bay Beach represented fewer than 1% of the annual estimated regional population of Silver Gulls in southeast Tasmania (mean 0.6 ± 0.5%). Including the 2017 data, the mean for 2009 to 2017 increased to 1.5 ± 2.9% of the annual estimated regional population of Silver Gulls in southeast Tasmania. The 2017 count at Blackmans Bay Beach comprised approximately 9% of the annual estimated regional population of Silver Gulls in southeast Tasmania in Winter 2017 (BirdLife Tasmania unpublished data).

Winter Silver Gull Proportion of SE Count Tasmania population %

2009 79 1.1 2010 36 0.4 2011 115 1.2 2012 15 1.2 2013 17 0.1 2014 20 0.1 2015 41 0.3 2016 24 0.2 2017 1000 9.2 Table 1. Numbers of Silver Gulls present on Blackmans Bay Beach from BirdLife Tasmania’s annual Winter Gull Counts and the proportion of annual estimated regional populations, expressed as a percentage (BirdLife Tasmania unpublished data).

4. Water Quality Data, Blackmans Bay South

The recreational water sampling in undertaken by Kingborough Council in conjunction with the DEP. The Derwent Estuary Program (DEP) provided data on Enterococcus counts from water samples collected from Blackmans Bay South (Table 2) for the period December 2011 to June 2017. The Kingborough Council provided data on Enterococcus counts from water samples collected from Blackmans Bay South (Table 3) for the period May 2017 to October 2017.

Further details of the sampling regime (typically monthly from December to March each summer) and the analytical procedures can be found at https://www.derwentestuary.org.au/beach-watch/.

The monthly data for Enterococcus counts (expressed as CFU/100ml) from Blackmans Bay Beach South and annual Winter Gull Counts from Blackmans Bay Beach for the period December 2011 to June 2017 are shown in Figure 3.

Overall, the Enterococcus count at Blackmans Bay Beach has increased in the period December 2011 to March 2016, and significantly so during the 2016/17 season (Table 2). A high Enterococcus count in December 2016 was attributed to a significant rainfall event that resulted in poor water quality at most beaches in the Derwent River.

In addition, the variances in the seasonal data have also increased, reflecting greater variability in the Enterococcus count data. The reasons for this increased variability are presently unknown, and it would be useful to compare the Blackmans Bay data with other data sets for the Derwent Estuary to see if similar increases in Enterococcus counts and the variances have been obtained elsewhere over the same time period.

BirdLife Tasmania Technical Report 2017 – 08 Page 5 Season Enterococci Blackmans Bay Beach South

2012/13 26 ± 22.2 2013/14 38 ± 47.8 2014/15 44 ± 69.8 2015/16 31 ± 37.4 2016/17 221 ± 493.3 Table 2. Enterococcus counts from Blackmans Bay South water samples. Source Derwent Estuary Program (DEP), unpublished data. The counts are expressed as seasonal means of monthly samples collected from December to March each summer. The monthly counts are expressed as CFU/100ml.

Date Enterococci Blackmans Bay Beach South

16-05-2017 20.0 22-05-2017 121.0 07-06-2017 262.0 20-06-2017 496.0 27-06-2017 135.0 04-07-2017 107.0 18-07-2017 3609.0 26-07-2017 10.0 01-08-2017 450.0 09-08-2017 183.0 16-08-2017 10 22-08-2017 10.0 29-08-2017 122.0 05-09-2017 64.0 09-09-2017 183.0 12-09-2017 10.0 20-09-2017 63.0 26-09-2017 10.0 03-10-2017 10.0 Table 3. Enterococcus counts from Blackmans Bay South water samples 2017. Source Kingborough Council unpublished data. The counts are expressed as CFU/100ml.

The highest counts of Enterococcus at Blackmans Bay Beach in the 2016/17 season were on 28 December 2016 (2005 CFU/100ml), 28 February 2017 (659 CFU/100ml) and 7 March 2017 (453 CFU/100ml), with lower counts in later samples taken in March 2017 (14, 21 and 28 March: 124, 178 and 31 CFU/100ml, respectively, DEP unpublished data). The high Enterococcus count (3609 CFU/100ml) on 18 July 2017 coincided with high numbers of Silver Gulls present on the beach, and with the total rainfall leading up to the date was <1.0mm in the preceding week (http://www.bom.gov.au/jsp/ncc/cdio/weatherData/av? p_nccObsCode=136&p_display_type=dailyDataFile&p_startYear=&p_c=&p_stn_num=094222).

The December 2016 count was during the Silver Gull breeding season, when the majority of gulls were on breeding islands (Figure 2 and see above), and with no records of elevated numbers of gulls at Blackmans Bay Beach. As noted earlier, this peak count was attributed to a significant rainfall event that resulted in poor water quality at most beaches in the Derwent River. The lower counts in late February and March 2017 and the peak in July 2017 are after the end of a typical breeding season, and before the 2017/18 breeding season for Silver Gulls in southeast Tasmania. The elevated Enterococcus count in February 2017 was after the arrival and subsequent increase in Silver Gulls on Blackmans Bay Beach (M Steele, Kingborough Council, pers. comm.).

With just one exception, the Enterococcus count data (Table 3) are relatively low and highly variable

BirdLife Tasmania Technical Report 2017 – 08 Page 6 throughout the months when Silver Gulls were present in high numbers. These data suggest that the Silver Gulls were not responsible, and that alternative source(s) should be investigated.

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0 0 Jan Jul Jan Jul Jan Jul Jan Jul Jan Jul Jan 2012 2013 2014 2015 2016 2017 Date Figure 3. Graph showing all Enterococcus count data from water samples collected from Blackmans Bay South, December 2011 - October 2017 (red symbols) and annual Winter Gull Count data for Blackmans Bay Beach for the 2013 to 2017 counts (blue symbols). Sources: Enterococcus counts from the Derwent Estuary Program and Kingborough Council (both sources, unpublished data) and Winter Gull Count data from BirdLife Tasmania, unpublished data. See also Tables 2 and 3.

5. Beaches, Enterococcus and Gulls

There is a vast global library of publications and data on bird fouling of water bodies, which are primarily focussed on issues around drinking water quality and recreational usage of water bodies. It is beyond the scope and intent of this report to summarise this material, and instead will focus specifically on studies of Enterococcus and gulls in coastal environments where relevant to the current situation at Blackmans Bay Beach.

The brief review will conclude with initial recommendations for Kingborough Council for their consideration, based on the results of this review. Implementation is believed to reduce the attractiveness of Blackmans Bay Beach to Silver Gulls during the non-breeding period.

For this report, a zoonosis (plural zoonoses) is defined as an infection or disease that is transmissible from animals (usually vertebrates) to humans under natural conditions.

Zoonoses can be caused by a range of disease pathogens such as viruses, bacteria, fungi and parasites. Zoonoses have different modes of transmission. In direct zoonosis, the disease is directly transmitted from animals to humans through media such as air (influenza) or through bites and saliva (rabies). In contrast, transmission can also occur via an intermediate species (known as vectors), which carry the disease pathogen without becoming infected. Significant zoonotic pathogens are Escherichia coli, Campylobacter, Enterococcidae, Caliciviridae, and Salmonella.

BirdLife Tasmania Technical Report 2017 – 08 Page 7 Enterococcus are currently used in Tasmania for measuring water quality, as they provide a better indicator of faecal contamination of water bodies (in both fresh and salt water), and a higher correlation with many of the human pathogens found in human sewage than do faecal coliforms. Faecal coliforms originate only from warm-blooded animals (Koskey et al. 2014), and identifying human and non-human sources of faecal coliforms presents significant challenges, in particular around time required for analyses and associated costs.

Enterococcus can cause various infections in humans ranging from urinary tract infections to chronic bacterial prostatitis and meningitis. Of increasing concern is the fact that Enterococcus exhibits a high level of intrinsic antibiotic resistance, resulting in extended treatments of antibiotics being required in humans.

Little research appears to have been undertaken in Australia on gulls as sources or vectors of zoonoses (but see Davies 1995 for an older review for zoonoses in Tasmanian wildlife), and no studies of the prevalence of Enterococcus in gulls in Australia are currently known.

Cragg and Clayton (1971) listed some bacterial flora of Northern Hemisphere gulls that included members of the Enterobacteriaecaea, Streptococcus and Staphylococcus amongst others. Extensive studies have reported Salmonella, Cryptosporidium, Giardia, Newcastle Disease Virus and avian influenza from gulls around the world (see Cooper 1990, Hatch 1996, Brown et al. 2006, Bogomolni et al 2008, Diel et al. 2012, Alley 2013, Alm et al. 2018.

A full microbial inventory of the organisms present in gull faeces has yet to be established despite their global distribution and potential role in adversely affecting water quality (Koskey et al. 2014).

Nadareski (2000) synthesized the available information on the sources, mechanisms, and risks of drinking water contamination from water birds. While the review was based in North America, the study found that overall, “… activities that provide healthy habitat usually help maintain—or at least do not significantly degrade—water quantity and quality for domestic use.”

Nadareski (2000) noted, that, “water birds have been implicated in the contamination of both large and small drinking water supplies.” Fouling of beaches by birds such as gulls is one potential source of human health concern (Koskey et al. 2014, Alm et al. 2018), but is dependent on the species, numbers involved and the duration of time spent on the site. Time of year will influence air and water temperatures, and tidal action is likely to wash the beach area(s) used by gulls at least once per day (depending on tidal regime), removing and/or diluting the volume of bird material to significantly lower levels.

Significantly fewer numbers and types of bacteria were found in dry gull droppings compared to wet, fresh droppings (Cragg and Clayton 1971), and Salmonella was absent from both dry and fresh gull droppings. Transmission to humans of a number of agents present in gull droppings would require direct contact, and this was considered, “unlikely” (Cragg and Clayton 1971).

Koskey et al. (2014) concluded that the human health risks associated with shorebird and waterfowl faeces on beaches were, “inherently lower than those from human faecal inputs”, and that the discharge of human sewage presented, “a greater radius of contamination risk” compared to small areas used by birds as roosts on beaches.

Similar conclusions were presented by Schoen and Ashbolt 2010 and Soller et al. (2010), both cited in Alm et al. (2018). More recently, Alm et al. (2018) were able to show gulls foraging at waste disposal sites acted

BirdLife Tasmania Technical Report 2017 – 08 Page 8 as vectors of various faecal micro-organisms to adjacent beaches, including Enterococcus, but acknowledged that this may be an infrequent occurrence.

6. Silver Gulls on Blackmans Bay Beach

The southeast Tasmania regional population of Silver Gulls is presently decreasing, currently estimated to be in excess of 10,000 individuals (BirdLife Tasmania, unpublished data), which is believed to be approximately 34% fewer than the peak recorded during the 2014 Winter Gull Count. This overall, regional decrease is in contrast with the increase observed at Blackmans Bay in recent years (Table 1, Figure 3).

This apparent contrast in trends is likely from a simple re-distribution of birds from an influx to Blackmans Bay Beach. Some aspect of Blackmans Bay Beach is attracting Silver Gulls there when previously the attraction was absent. Alternatively, the Silver Gulls are being displaced/disturbed elsewhere and adopted Blackmans Bay Beach as an alternative to their preferred roosting choice. In the absence of additional information on surrounding roosts, the cause(s) of the influx of Silver Gulls to Blackmans Bay cannot be determined.

Whether the increase in Silver Gulls is directly associated with the increase in Enterococcus counts at Blackmans Bay requires further sampling before any causative link can be established. Given the high number of variables involved, assessing and managing the potential impacts and concerns for human health associated with Silver Gull use of Blackmans Bay Beach require site-specific sampling, data collection and analyses (Fogarty et al. 2003, Koskey et al. 2014).

Numerous reports of, “approximately” 2000 Silver Gulls were received by Kingborough Council during the winter months of 2017, equating to the non-breeding season of Silver Gulls in southeast Tasmania (see above). A site visit on 11 August 2017 recorded 2000 Silver Gulls sitting on the water to approximately 100m offshore at the southern end of the beach (see Frontispiece).

A number of birds were observed drinking the runoff from a small Council drain approximately 200m north of the southern end of the beach (Figure 4) on both visits. On 11 August, approximately 100 of the 2000 Silver Gulls are in or in close proximity to the runoff, while on 17 September there were fewer Silver Gulls present both on the beach and at the runoff.

Gulls can generate between 1.7% and 4.2% of their body mass each day in faeces (Hatch 1996). A Silver Gull weighs between 265g and 315g, so the range of faecal material produced per day ranges between 4.5g and 13.2g. A flock of 1000 Silver Gulls would generate between 4.5 – 13.2kg per day, and a flock of 2000 birds as reported frequently during the 2017 winter months would generate between 9.0 and 26.2kg per day.

These quantities are insignificant compared to the sewage discharged from the adjacent Blackmans Bay Sewage Treatment Plant. There are presently no data available on the Enterococcus counts in Silver Gull faeces and in the human sewage discharged from the Blackmans Bay Sewage Treatment Plant, so no assessment of the relative contributions from these two sources is presently possible.

BirdLife Tasmania Technical Report 2017 – 08 Page 9

Figure 4. Silver Gull drinking stormwater runoff from Council drain at Blackmans Bay Beach, 17 September 2017. Picture ©Eric Woehler, BirdLife Tasmania.

7. Conclusions

There are no data to draw on for the relationship between gulls and Enterococcus in Australia, and extreme caution must be exercised before transferring results from other species in other regions of the world to Silver Gulls at Blackmans Bay. This is due to the wide range of bacterial micro-organisms present, the behaviours of the Silver Gulls and the various environmental parameters (such as air and water temperatures, tidal regime and solar radiation) that can influence the persistence of the micro-organisms present on site (eg Fogarty et al. 2003).

Specifically:

1. The peak counts of Enterococcus appeared before the arrival of the Silver Gulls at Blackmans Bay Beach, resulting from an unusual rainfall event, suggesting that alternative source(s) were responsible, rather than the Silver Gulls acting as vectors for the Enterococcus.

2. Kingborough Council may wish to investigate the abundance and type(s) of Enterococcus in the discharge from the adjacent Blackmans Bay Sewage Treatment Plant over a 12-month period as a potential alternative source of the Enterococcus detected in the Derwent River at Blackmans Bay.

3. These investigations may provide additional information on any links between the discharge and detection at the beach over the period of investigation. The investigation should also include data on river flows that may contribute to an understanding of local hydro-dynamics (eg Wild-Allen et al. 2013, Wild-Allen and Rayner 2014).

4. The absence of cloacal swabs from Silver Gulls or from fresh droppings prevent any testing or establishment of a causative link between the birds and high Enterococcus counts.

5. At present, there are no data to support the proposal that the high Enterococcus counts recorded by DEP at Blackmans Bay Beach originated from Silver Gulls present during the winter months.

BirdLife Tasmania Technical Report 2017 – 08 Page 10

6. The cause(s) of the influx of Silver Gulls to Blackmans Bay during 2017 cannot be determined at this time.

8. Recommendations

Consideration by Kingborough Council of the following recommendations may alleviate community concerns about the potential for human health issues in the future.

1. The presence of the stormwater runoff at the southern end of Blackmans Bay is likely to act as an attractant to the gulls. While freshwater is not essential for Silver Gulls, they make conspicuous use of any sources of freshwater for bathing, drinking and washing/preening. Sealing the open stormwater runoff and extending the drain to below low water will reduce the potential use of the runoff to Silver Gulls (and likely other species of birds).

2. If Silver Gulls return and their numbers increase in 2018 as seen in 2017, then consideration should be given by Council to collect water samples from the Derwent River as per the usual DEP protocols to allow for an assessment of Enterococcus and other microorganisms while the Silver Gulls are present.

In addition, the capture of Silver Gulls should be considered to obtain concomitant cloacal swabs that could allow for the collection of data to investigate if the Silver Gulls are acting as vectors for various microorganisms at Blackmans Bay Beach. In the absence of cloacal swabs, collection of fresh gull droppings may provide an alternative source of data.

3. BirdLife Tasmania would discourage any efforts to disperse or discourage the Silver Gulls by deliberate human disturbance of the roosting birds on Blackmans Bay Beach. It is likely that such efforts would result in (a) little change in their behaviour, (b) a re-location to an adjacent area of Blackmans Bay Beach or another foreshore of some or all of the birds, and (c) no long-term, strategic ‘solution’ to the issue.

9. Acknowledgements

Thanks to I Visby (Derwent Estuary Program) for making the Enterococcus data available for this report. M Steele (Kingborough Council) instigated this study, provided unpublished count data and was helpful in providing additional details while patiently waiting for the report. Dr V Ruoppolo DVM reviewed the draft and provided useful comments on an earlier draft.

BirdLife Tasmania Technical Report 2017 – 08 Page 11 10. References cited

Alley M 2013. Wildlife in New Zealand as a source of zoonoses. Proceedings of the New Zealand Veterinary Association Conference 2013, pp 153-160. Alm EW, Daniels-Witt QR, Learman DR, Ryu H, Jordan DW, Gehring TM, Santo Domingo J 2018. Potential for gulls to transport bacteria from human waste sites to beaches. Science of The Total Environment 615,123-30. Bogomolni AL, Gast RJ, Ellis JC, Dennett M, Pugliares KR, Lentell BJ, Moore MJ 2008. Victims or vectors: a survey of marine vertebrate zoonoses from coastal waters of the Northwest Atlantic. Diseases of aquatic organisms 81, 13 - 38. Brothers, N., Pemberton, D., Pryor, H., and Lucieer, V. L. 2001. Tasmania’s Oﬀshore Islands: seabirds and other natural features. Tasmanian Museum, Hobart. Brown JD, Stallknecht DE, Beck JR, Suarez DL, Swayne DE 2006. Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerging infectious diseases 12, 1663 – 1670. Cooper JE 1990. Birds and zoonoses. Ibis 132, 181-191. Cragg J, Clayton YM 1971. Bacterial and fungal flora of seagull droppings in Jersey. Journal of clinical pathology 24, 317-319. Diel DG, Miller PJ, Wolf PC, Mickley RM, Musante AR, Emanueli DC, Shively KJ, Pedersen K, Afonso CL 2012. Characterization of Newcastle disease viruses isolated from cormorant and gull species in the United States in 2010. Avian diseases 56, 128-133. Fogarty LR, Haack SK, Wolcott MJ, Whitman RL 2003. Abundance and characteristics of the recreational water quality indicator bacteria Escherichia coli and enterococci in gull faeces. Journal of Applied Microbiology 94, 865-878. Hatch JJ 1996. Threats to public health from gulls (Laridae). International Journal of Environmental Health Research 6, 5-16. Koskey AM, Fisher JC, Traudt MF, Newton RJ, McLellan SL 2014. Analysis of the gull fecal microbial community reveals the dominance of Catellicoccus marimammalium in relation to culturable Enterococci. Applied and environmental microbiology 80, 757-765. Nadareski CA 2000 Water birds. In Dissmeyer GE. Drinking water from Forests and Grasslands. USDA Forest Service General Technical Report SRS-39, Asheville, North Carolina, pp 164-168. Wild-Allen K, Rayner M. Continuous nutrient observations capture fine-scale estuarine variability simulated by a 3D biogeochemical model 2014. Marine Chemistry 167, 135-149. Wild-Allen K, Skerratt J, Whitehead J, Rizwi F, Parslow J 2013. Mechanisms driving estuarine water quality: a 3D biogeochemical model for informed management. Estuarine, Coastal and Shelf Science 135, 33- 45.

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