Marine and Freshwater Resources Institute The ...

Marine and Freshwater Resources Institute Report No. 33

The distribution, abundance and population dynamics of the exotic seastar Asterias amurensis during the first three years of its invasion of Port Phillip Bay (incorporating a report on the Bay Pest Day, 2 April 2000).

G. D. Parry and B. F. Cohen

April 2001

Marine and Freshwater Resources Institute Report No. 33

The distribution, abundance and population dynamics of the exotic seastar Asterias amurensis during the first three years of its invasion of Port Phillip Bay (incorporating a report on the Bay Pest Day, 2 April 2000).

G. D. Parry and B. F. Cohen

April 2001

Marine and Freshwater Resources Institute PO Box 114 Queenscliff 3225

Copyright © Department of Natural Resources and Environment 1999 This work is copyright. Apart from any use under the Copyright Act 1968, no part may be reproduced by any process without written permission.

ISSN: 1328-5548 ISBN: 0 7311 4820 7

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Librarian Marine and Freshwater Resources Institute PO Box 114 Queenscliff VIC 3225 Phone: (03) 5258 0259 Fax: (03) 5258 0270 Email: [email protected]

Preferred way to cite this publication: Parry, G.D. and Cohen, B.F. (2001) The distribution, abundance and population dynamics of the exotic seastar Asterias amurensis during the first three years of its invasion of Port Phillip Bay (incorporating a report on the Bay Pest Day, 2 April 2000). Marine and Freshwater Resources Institute Report No. 33. (Marine and Freshwater Resources Institute: Queenscliff).

General disclaimer: This publication may be of assistance to you but the State of Victoria and its employees do not guarantee that the publication is without flaw of any kind or is wholly appropriate for your particular purposes and therefore disclaims all liability for any error, loss or other consequence which may arise from you relying on any information in this publication.

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Summary This report describes the population dynamics of Asterias amurensis during the first three years of its invasion of Port Phillip Bay. Patterns of mortality, growth and reproduction were studied in detail during the third year of the invasion, and were inferred from size frequency distributions for the second year of the invasion, and with less confidence for the first year of the invasion. Detailed studies were undertaken at 12 plots sampled regularly between July 1999 and September 2000, and changes to the distribution and abundance of the first 3 age cohorts were monitored by baywide surveys conducted between March 1999 and November 2000. Most Asterias amurensis in Port Phillip Bay spawned between mid-July and midSeptember during 1999, but spawning commenced in mid-June during 2000. Settlement of juvenile A. amurensis occurred between August and November during 1999 and peaked in mid-September, indicating that the duration of larval phase was approximately 60 days. Since the first Asterias amurensis was found in Port Phillip Bay in 1995, the population grew to 340,000 (+ 60,000 SE) in early 1998, to 26 (+ 4 SE) million in 1999, and to 96 (+ 14 SE) million by early 2000. During 2000 the population size of the first 3 cohorts appears to have declined to 75 (+ 15 SE) million, largely due to high mortality of the 1999 cohort in the main area of infestation in the north east of the bay. In the 3 years since Asterias amurensis spawned in the bay, the main area of infestation has remained in the north east of the bay in waters deeper than 15 m. Further increases in the population of A. amurensis in the bay are likely once larvae are transported to areas in the south and west of the bay. In the main area of infestation, growth and reproduction of A. amurensis declined markedly between years 2 and 3 of the invasion, although mortality rates have remained low. In this area the exponential phase of population growth may be nearly complete as food appears to be limiting further growth and reproduction. The population in the main area of infestation may decline in the future, but should this occur, the preferred prey of A. amurensis are likely to have become rare or locally extinct, and the benthic community structure in this area is likely to be permanently altered.

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Introduction The huge economic costs resulting from the invasion of the Great Lakes by the zebra mussel, Dreissena polymorpha, (Griffiths 1991; Strayer 1991) and the Black Sea by the ctenophore Memiopsis leidyi (Vinogradov 1989) has raised the level of international concern for problems posed by the translocation of marine species. Within Australia, the establishment of the exotic northern Pacific seastar Asterias amurensis in Tasmania similarly attracted a great deal of publicity and significantly increased awareness of the impact of exotic marine species. During the 1990s, A. amurensis became the most conspicuous organism in the Derwent estuary and by 1995 its population was approximately 28 million (Grannum 1996). Field studies in the Derwent confirmed that A. amurensis preyed on a wide range of native fauna (Grannum 1996) and that densities were as high as 24/m2 (McLoughlin and Thresher 1994). Consequently, A. amurensis was considered to have the potential to profoundly affect native communities in southern Australia (Ross and Johnson 1998). Asterias amurensis is native to the coasts of Japan and southeastern Russia (Ward and Andrew 1995) and was probably transported to the Derwent estuary in S.E. Tasmania in the ballast of vessels. Comparison of allozymes between the Tasmanian population and native populations suggest that central Japan was the most likely source of the Tasmanian population (Ward and Andrew 1995). The first confirmed specimen of A. amurensis in the Derwent was collected during October 1986, but it was not correctly identified until 1992 (Zeidler 1992). Consequently, there were no studies undertaken during at least the first six years of the invasion in the Derwent. During the mid 1990s Asterias amurensis were confined to the Derwent estuary. Hydrological modelling suggested that this limited distribution was the result of limited larval dispersal (Davenport and McLoughlin 1993). However, by 2000 the distribution of A. amurensis in Tasmania still had not extended significantly beyond the Derwent estuary. More recent modelling (C. Johnson, Univ Tasmania, pers comm) suggests that most larvae are flushed from the estuary, hence biological factors may be limiting the spread of A. amurensis beyond the estuary. Between 1995 and 1997 four adult Asterias amurensis were collected from Port Phillip Bay and in early 1998 many juveniles were found (Parry et al. 2000). Genetical studies indicate that the Port Phillip Bay population probably came from the Derwent (Murphy and Evans 1998). These two populations are 700 km apart and no A. amurensis have been found at intermediate locations. This distribution pattern and the prevailing currents (Bruce 1998) suggest that natural dispersal of larvae from the Derwent to Port Phillip Bay is very unlikely. Vessels travelling between Hobart and Melbourne are the most likely vector, but it is uncertain whether A. amurensis were introduced as larvae in ballast water or as adults. That the first four A. amurensis found in Port Phillip Bay were 10s of km apart and all were adults spawned in at least two different years (Parry et al. 2000), suggests that these first arrivals may have been transported as adults. In contrast, when juveniles were first found in early 1998, many individuals of the same age were found in the same region. Such a distribution pattern would be expected if these seastars resulted from larval settlement following a successful spawning in the bay, or possibly following the discharge of ballast water containing a high density of A. amurensis larvae.

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Most studies of exotic species do not commence until a population is large enough to present an economic or environmental problem. Typically this occurs once the exotic species is well established, some years after the initial invasion. Studies in the Derwent followed this typical pattern and did not commence until Asterias amurensis had been established for approximately a decade (Byrne 1997). However the presence of A. amurensis in the Derwent and its apparent impact there (McLoughlin and Thresher 1994) heightened awareness of the risk of its translocation to Port Phillip Bay. This resulted in the early detection of A. amurensis in the bay and the commencement of ecological studies during the early phase of its establishment. Typically the ‘environmental resistance’ (Chapman 1931) due to native predators, parasites, pathogens or competitors increases as an invasion proceeds. Even where the establishment of the new exotic species has been facilitated by previously established exotic species (Simberloff and Von Holle 1999), a temporal increase in resistance is expected. Typically, during the establishment phase (sensu Vermeij 1996) there will be a decrease in resources, as the exotic species progressively consumes the most easily harvested food, or increasingly saturates its preferred habitats. As an invasion proceeds and an exotic species becomes progressively integrated into its new community, native predators (or parasites) may become more effective as they learn that the newly introduced exotic is a valuable food source, or as their populations expand or undergo adaptation in response to the increased prey provided by the exotic species. Such changes may slowly diminish the impacts of the exotic species over time. Exotic species that cause the most devastating impacts include species that modify their habitat in ways that further enhance their populations. For example, in inland Australian waters, exotic European carp increase the turbidity of billabongs, which disadvantages native species (King et al 1997; Robertson et al. 1997). Predators such as Asterias amurensis, which feed on a very wide size range of prey (Grannum 1996), may alter trophic relationships so that their impact increases during the years immediately following their establishment. For example, adult A. amurensis may eliminate the predators of newly-settled juvenile A. amurensis, facilitating further population increases. Only studies conducted during the early years of the invasion, when predators of young A. amurensis still remain, are likely to identify such changes. Thus ecological studies in the early phase of an invasion assume considerable importance, as studies undertaken later may fail to recognise a native predator that was initially an important cause of mortality, but whose importance subsequently diminished as it was consumed by the invader. The present study aimed to identify patterns of distribution, growth, reproduction and mortality of Asterias amurensis in Port Phillip Bay, during the early years of the invasion. Specifically, the objectives of the study were to: (1) Describe the population dynamics in Port Phillip bay in detail during 1999/00 and in less detail during 2000/01. (2) Determine the distribution and abundance of all identifiable age cohorts of A. amurensis in Port Phillip Bay during 1999 and 2000. (3) Determine temporal changes in condition during 1999/2000 and spatial differences during 2000/01.

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The study complements other studies examining the influence of hydrodynamic factors on the distribution of Asterias amurensis (Parry et al. 2000) and of biological factors which may be responsible for the mortality and growth patterns noted in this study (Parry et al. in preparation). Patterns of mortality and growth were studied in detail during the third year of the invasion, and were inferred from size frequency distributions for the second year of the invasion, and with less confidence for the first year of the invasion. This report describes the population dynamics of Asterias amurensis at 12 study plots between July 1999 and September 2000, and changes to the distribution and abundance of the first three cohorts of A. amurensis that recruited in Port Phillip Bay during 1997, 1998 and 1999. This report also includes the results of the Bay Pest Day, a community event involving 200 divers, that was, in part, designed to provide information of the population density of Asterias amurensis to enable calibration of the dredge used to sample A. amurensis throughout this study. Methods Field studies In all field studies Asterias amurensis were sampled using the same 2.7m wide Peninsula scallop dredge (Hughes 1973), covered by 25 mm mesh to catch small seastars. All estimates of field densities were based on the number of seastars collected in a nominally 60 sec dredge tow. The dredge was towed at a speed of 5.7+ 0.3 knots, and the duration of each tow was measured from the time the brake was applied to the dredge tow cable on deployment, until the commencement of the retrieval of the dredge. The length of each tow was calculated from the vessel’s position when the brake was applied to the dredge tow cable and its position when retrieval of the dredge commenced 60 sec later. Vessel positions were recorded using differential GPS. The area swept by the dredge was estimated from the length of the tow and the width of the dredge. On average, the length of a nominally 60 sec tow was 170 m, therefore, all abundance estimates were standardised to tows of 170 m. Dredge efficiency On 7 April 2000, 20 tows of the scallop dredge were undertaken on a 500 m  500 m plot in 17 m depth near Mordialloc Creek. Each dredge tow was nominally of 60 sec duration. Two forward looking video cameras were located on the dredge and each had a field of view of approximately 80 cm of seabed. Video cameras were used to determine the behaviour of the dredge and the duration of contact between the dredge and the seabed during each nominally 60 sec tow. Of the 20 dredge tows, poor underwater visibility meant that observations were only possible on 11 tows. This video technique could not be used to estimate the abundance of Asterias amurensis in the path of the dredge, as the dredge was travelling too quickly for most A. amurensis to be observed. On 13 June 2000, a video mounted on a sled was used to estimate the density of Asterias amurensis in a plot 500 m  500 m immediately adjacent to the area

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surveyed by dredge on 7 April 2000. The sled was towed at 1.5-2 knots across the plot from East to West, along 10 transects approximately 50 m apart. Each tow was approximately 500 m in length, and was measured accurately using differential GPS on the towing vessel. The video recorded a track 0.75 m wide. When the tape was viewed all A. amurensis in two size classes (10 cm) were counted. These two size classes were chosen as the seastar population consisted of two ageclasses, those less than 1 year old which were mostly < 9 cm, and those nearly two years old, which were mostly >11 cm. There were few seastars 10 cm in diameter. Small A. amurensis could not be counted reliably on the video as they were difficult to see when covered by a fine layer of sediment, but A. amurensis >10 cm were seen readily. On 14 June 2000, on the same plot used for the video survey the previous day, the number of Asterias amurensis in two size classes (10 cm) caught in each of 20 nominally 60 sec tows was recorded. The density of A. amurensis was calculated from the estimated area swept during each dredge tow, as described previously. Population dynamics on study plots The dynamics of Asterias amurensis populations were investigated at 12 one km2 plots, located at depths of 15 m, 17 m, and 20 m along four transects near Aspendale, Brighton, Mordialloc and Werribee (Fig 1). These plots were chosen to include areas of high A. amurensis density (Aspendale 17 & 20 m sites, Brighton 17 & 20 m sites, Mordialloc 15, 17 & 20 m plots) and areas near the boundaries of the distributional range of A. amurensis where densities were low (Aspendale 15 m, Brighton 15 m, Werribee 15, 17 & 20 m plots). Plots on the Aspendale and Brighton transects were always sampled on the same date, as were those on the Mordialloc and Werribee transects. These transect pairs were sampled alternately at intervals of 2-4 weeks. Each plot was sampled on 10 occasions between 24 August 1999 and 8 September 2000 (Appendix 1). On each sampling date, three 60 sec dredge tows were undertaken at haphazard locations within each plot, but the positions of all dredge tows were recorded using DGPS. The diameters of Asterias amurensis caught in each dredge tow was measured to the nearest 5 mm. When more than 100 were caught, a subsample of 100 was measured and the remainder counted. Where A. amurensis were regenerating arms, the diameter was estimated using the non-regenerating arms. Reproduction and condition The time of spawning and the seasonal changes in energy reserves in the pyloric caecae were determined by collecting 15 female Asterias amurensis from within the north eastern region of Port Phillip Bay (17-20 m depth) where the main area of infestation occurred. Females were collected every 2-3 weeks during the spawning season and less frequently at other times. After detailed population dynamics studies commenced in August 1999, all A. amurensis were collected from a subset of those study sites used for population dynamics studies (17, 20 m Mordialloc, 17, 20 m Aspendale, or 17, 20 m Brighton study sites, Fig 1). The diameters of these seastars were measured, their ovaries and pyloric caeca were dissected and the dry weights of

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these components and the total dry body weight determined by drying at 85 oC for 48 h. Plots of ovary weight (O) vs seastar diameter (D) for each sampling date indicated that, beyond the diameter at which sexual maturity is attained (11 cm, Fig 2, Morrice 1995), the two variables are linearly related. Regressions of O vs D were calculated so that all passed through the point (11.0, 0). Therefore, at each sampling date, equations of the form O = b (D-11.0) were obtained. Seasonal changes in the average size of ovaries are reflected in the values of the gradient, b, of these equations. Seasonal changes in the condition of Asterias amurensis were determined from changes in the ratio of the dry weight of pyloric caeca/total dry weight of A. amurensis. On each sampling date, pyloric caecae were removed and weighed from all the seastars used for analysis of seasonal changes in ovary weight. Settlement A 1 mm mesh plankton net (300 mm diameter, 1 m length) was attached to the rear of the scallop dredge to sample the sediment plume for newly-settled Asterias amurensis (Currie and Parry 1996). Samples were collected on the 12 study sites during 60 sec dredge tows and later sorted and the diameter of each A. amurensis measured. A. amurensis were identified by reference to unpublished images of newly-settled A. amurensis from the Derwent provided by C. Sutton, CSIRO. To determine the main period of settlement, samples collected from all dates were considered and those less than or equal to 3 mm in diameter were considered to have settled recently. The mean numbers of these recently settled A. amurensis caught /60 sec dredge tow were plotted against time to determine the main period of settlement. Growth and mortality Growth and mortality on each of the 12 study plots were estimated from size frequency distributions collected on 10 occasions between August 1999 and September 2000 (Appendix 1). Size frequency distributions of Asterias amurensis at each study plot and sampling date were separated into three age cohorts (Appendix 1). The oldest cohort (1997 cohort) was spawned in Port Phillip Bay in mid 1997, although this cohort was not noticed until individuals had grown to a diameter of 5 cm in early 1998 (Parry et al. 2000). When detailed studies commenced in August 1999, the A. amurensis population consisted of two cohorts, one spawned in 1997 and another spawned in 1998. By October 1999, individuals from the 1999 cohort, spawned in mid July 1999, were large enough to be detected in dredge samples. In approximately half the size frequency distributions on the study plots, it was possible to distinguish a group of larger individuals that probably resulted from the 1997 spawning. These individuals were always > 20 cm diameter. But for the remainder of the size frequency distributions analysed, the 1997 and 1998 cohorts could not be separated confidently. In these latter cases, all Asterias amurensis > 20 cm diameter were assigned to the 1997 cohort. Between November 1999 and May 2000 the 1998 and 1999 cohorts were clearly distinguishable as the size frequency distributions of each cohort did not overlap

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significantly. However, between May 2000 and August 2000 the size frequency distributions of the 1998 and 1999 cohorts partially overlapped. During this period, separation of the 1998 and 1999 cohorts was achieved using the normsep routine of the computer package FISTAT. This program indicated each annual cohort consisted of up to three sub-cohorts, probably corresponding to different spawning and settlement events within a single breeding season. In this report all cohorts spawned in the same year have been considered collectively. Growth of each of the three cohorts (1997, 1998, 1999) was estimated on each study plot from changes in the diameter of each cohort between August 1999 and September 2000. Regressions of diameter of each cohort against date were calculated for each study plot. ANOVA was used to test whether the gradients of these regressions were significantly different from zero, and ANCOVA was used to test whether seastars from different depths and sites had significantly different growth rates. Mortality rates of each of the three cohorts (1997, 1998, 1999) were estimated on each study plot from changes in the density (Number caught/170 m tow length) of each cohort between August 1999 and September 2000. Mortality rates of each cohort were estimated from regressions of loge N against date for each study plot. The mortality rate of the 1999 cohort was determined for the period March-September 2000, after recruitment had ceased. ANOVA was used to test whether the gradients of these regressions were significantly different from zero, and ANCOVA was used to test whether seastars from different depths and sites had significantly different mortality rates. To determine whether growth of Asterias amurensis was density dependent, growth ( diameter) of the 1998 and 1999 cohorts during their first year was plotted against the mean biomass of A. amurensis on each plot during that year. The mean biomass on each plot during the 1999 cohort’s first year (July 1999 - July 2000) was calculated directly from the 10 size frequency distributions measured on these plots during this period (Appendix 1) and the relationship between seastar diameter and dry weight [Log10(Dry weight)= -1.729 + 2.3728Log10(Diameter), N= 546]. The mean biomass of the 1998 cohort during its first year was estimated to be 50% the biomass of this cohort attained by July 1999. The July 1999 biomass of the 1998 cohort was estimated from the size frequency distribution measured on the date closest to July 1999 and the relationship between diameter and dry weight. Note that the 1998 cohort probably had low mortality during its first year, as its mortality was low in its second year, and that the 1997 cohort had a very low abundance on all plots. Distribution, abundance, growth and mortality of Asterias amurensis throughout Port Phillip Bay The distribution and population density of Asterias amurensis was determined by collecting seastars in 60 sec dredge tows at sites throughout Port Phillip Bay between July 1999 and November 2000. On average, the length of a nominally 60 sec tow was 170 m. Consequently, all abundance estimates were standardised to tows of 170 m, then corrected to allow for the efficiency of the dredge (115%, see below) during a 60 sec tow.

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Extensive baywide surveys were undertaken during three periods (March-November 1999, December 1999-March 2000, and April-November 2000), although in each of these time periods the majority of the surveying occurred in the last month of the survey period (i.e. during November 1999, March 2000 and November 2000). The diameter of all Asterias amurensis collected in each dredge tow was measured at each site, except where more than 100 individuals were collected in which case 100 were measured and the remainder counted. The sites sampled during each baywide survey were selected based upon the available knowledge of the distribution of A. amurensis at the time, the total number of sites that could be visited in 2-3 days, and most efficient mix of vessel courses to ensure that the main areas of the infestation, including its boundary, were well defined. Size frequency distributions of Asterias amurensis at each site sampled were separated into the age cohorts, as described for studies of population dynamics. Until October 1999 only two cohorts (1997, 1998) were present in dredge samples. After October 1999, the 1999 cohort also appeared in dredge samples. Separation of the 1997 and 1998 cohorts was approximate only. Separation of the 1998 and 1999 cohorts was based on size frequency distributions and, for samples collected in November 2000, on whether any A. amurensis had been found in the same region in the previous year. Field observations throughout the study suggested that Asterias amurensis from regions with a high food supply had wider arms than those from regions with a low food supply. This pattern was particulary evident in small populations that were found in south western Port Phillip Bay during November 2000. These populations consisted of seastars with wide arms, which were often collected in the dredge in a humped feeding position with large quantities of the fragile epibenthic bivalve Electroma georgiana upon which they appeared to have been feeding. During November 2000, seastar diameter could not be used to reliably assign seastars from widely separated regions of the bay to the 1998 or 1999 cohorts. At this time, seastars from the 1999 cohort in regions where no seastars had been detected in the previous year, were a similar size to those from the 1998 cohort and much larger than those from the 1999 cohort in the main area of infestation. To provide additional evidence that the large seastars found in areas where no seastars had been found during the previous year were, in fact, fast-growing seastars from the 1999 cohort, an index of condition based on the ratio of arm width to diameter was calculated for seastars from all sites sampled in November 2000. The diameter and maximum arm width of 25 Asterias amurensis (or all those collected when N10 cm diameter with an efficiency of 115% (Table 2). However the dredge clearly cannot collect more than 100% of seastars in its path and this was confirmed by observations obtained by video cameras placed on the scallop dredge. A small number of seastars passed over the top of the dredge and the dredge lost contact with the seabed approximately 9% of the time (Table 3), when seastars could not be caught. The video cameras also showed that a nominally 60 sec dredge tow remained in contact with the seabed for an average of 74 seconds (Table 3). The additional 14 sec of contact with the seabed was the result of the deployment and retrieval phases of the dredging. During these phases the dredge speed may differ from the vessel speed; therefore the distance covered in this 14 sec could not be estimated accurately. But if it is assumed that the dredge travels at constant speed while on the seabed, then the distance travelled will be 23% greater than in the nominally 60 sec deployment. The measured dredge efficiency during a 60 sec tow suggests that the dredge collects about 93% (115/123) of seastars in its path. However, as the dredge was off the seabed for approximately 9% of the time, this suggests that the dredge collects nearly 100% of seastars in its path when it is in contact with the seabed. The same dredge collects 4555% of scallops in its path (Currie and Parry 1999) and seastars should be collected more efficiently, as, unlike scallops, they cannot swim to avoid the dredge nor are they usually found in hollows in the seabed. Small seastars could not all be seen using the video sled. Hence the efficiency of the modified scallop dredge collecting Asterias amurensis 15 m and 15 m and