This article was published by Springer-Verlag Berlin Heidelberg, and the final publication is available at http://link.springer.com/article/10.1007/s00227-014-2441-7 1
Distribution and seasonal abundance of Polygordius spp. (Class Polychaeta: Family
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Polygordiidae) exo- and endolarvae in the southern Mid-Atlantic Bight, USA
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Patricia A. Ramey-Balcı1,* and Julie W. Ambler2
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Center, Environment and Cleaner Production Institute, Marine Group, Gebze, Kocaeli 41470,
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Turkey. Email:
[email protected]
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TÜBİTAK (The Scientific and Technological Research Council of Turkey), Marmara Research
Department of Biology. Millersville University, Millersville, PA 17551, USA
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Running page head: Polygordius exo- and endolarvae USA
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Key words: Polygordius jouinae, COI, life history, plankton, recruitment, barcode
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Abstract
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The importance life history plays in understanding population dynamics and the functional roles
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of species for predicting climate change scenarios are well established. Yet, in the marine
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environment the complete life history is unknown for many species, especially the link between
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morphologically and ecologically distinct planktonic larvae, and their corresponding benthic
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adult forms. Integration of meroplankton abundance, benthic adult species, larval morphology,
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and molecular data was employed to unravel the complete life history of Polygordius, a dominant
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polychaete in sandy shelf sediments of the Mid-Atlantic Bight. Polygordius species are unusual,
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having two distinct planktonic larval forms: an exolarva and an endolarva. Extensive sampling in
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the southern Mid-Atlantic Bight with careful preservation of meroplankton (2006−2007) revealed
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the identity of multiple stages of exo- and endolarvae, and their spatial, seasonal, and vertical
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distribution. Molecular and morphological evidence indicated exolarvae are Polygordius jouinae,
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and endolarva are an undescribed species. Structure and development of these larvae differed
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greatly. Polygordius jouinae exolarvae were found off Delaware Bay to North Carolina. At some
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stations, they were abundant, with densities up to 4,013 m-3, comprising > 90% of the total
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meroplankton. Exolarvae spent up to a month in the plankton starting in March/May depending
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on year, settlement began in July when larvae were at least 2 mm in length, and by October were
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no longer observed in the plankton. These findings are consistent the distribution patterns and life
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cycle known for adults. This is the first report of endolarvae north of Cape Hatteras.
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Introduction
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Most marine benthic invertebrates have complex life histories which include planktonic larval
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stages that metamorphose into morphologically and ecologically distinct juveniles and adults
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(e.g., Thorson 1950; Giese and Pearse 1974; Pechenik 1999). Many marine invertebrate larvae
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are still undescribed (Emlet et al. 2009), and the links between larvae and their corresponding
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adult forms are unknown for many species. Knowledge of the complete life history of benthic
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invertebrates, and the biological and physical factors affecting both larvae and adults is necessary
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for understanding their population dynamics and functional roles in marine ecosystems (Eckman
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1996). Relative abundances of benthic macrofaunal invertebrates have increasingly been used to
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assess the biological integrity of marine systems (e.g., Borja et al. 2000; Ramey et al. 2011;
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Dauvin et al. 2012; Garmendia et al. 2012), and have become essential for international
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monitoring and assessment programs and policies (e.g., Borja 2004; Van Hoey et al. 2010). Some
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species are regarded as bio-indicators of relatively “pristine” environments or highly impacted
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eutrophic areas, with some notoriously described as opportunistic (e.g., Capitella teleta, Blake et
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al. 2009) or highly invasive (see http://www.issg.org/) depending on where they occur.
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Along the east coast of the United States Polygordius spp. (Family Polygordiidae) are the
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predominant benthic macrofaunal organisms in sandy, continental shelf sediments with high
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levels of physical disturbance by waves and currents (Ramey 2008a, b; Grassle et al. 2009). Only
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one species belonging to this genus, Polygordius jouinae Ramey, Fiege, and Leander 2006, has
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been described from this region although more remain to be described (Ramey-Balcı unpubl pers
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obs). Adult Polygordius spp. not attributable to P. jouinae have been studied in samples
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distributed from Virginia to Tampa Bay, Florida (Ramey-Balcı unpubl pers obs). Chaetogordius
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canaliculatus Moore 1904, a putative species in the only other genus in the Polygordiidae, was 3
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described off Cape Cod from fragmented material, and thus is regarded as an invalid taxon
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(Hermans, 1969; Westheide 1990; Rota and Carchini 1999). Polygordius jouinae is distributed in
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bays and harbours from Massachusetts to southern New Jersey (42°N to 39°N) to a maximum
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depth of 152 m on Georges Bank (Ramey et al. 2006). Extensive benthic sampling along coastal
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New Jersey from Sandy Hook to Cape May in 2007 and 2009 (shore to 3 nm offshore, n = 153
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samples) found Polygordius spp. (likely P. jouinae) to be numerically dominant, making up 34%
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and 70% of the total macrofaunal abundances (0.5-mm and 0.3-mm mesh sieves respectively).
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The highest density was 10,942 individuals 0.04 m-2 (Ramey et al. 2011). Several observations
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suggest that Polygordius spp. may be useful indicators of changing environmental conditions
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(Ramey 2008b; Grassle et al. 2009). The distribution and density of P. jouinae is affected by
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sediment composition and associated increases in organic loading (Ramey et al. 2006; Ramey
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2008b) showing a clear preference for coarse sandy sediments with little or no fine fraction (see
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Table 2 in Ramey et al. 2006). Moreover, similar long-term trends in temporal patterns of
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abundance of this taxon in two systems at the northern and southern ends the known distribution,
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may have been influenced by large-scale oceanographic processes and climate variability due to
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phenomena such as the North Atlantic Oscillation (NAO) or the Atlantic Multidecadal
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Oscillation (AMO) (Ramey 2008c; Schofield et al. 2008).
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Until now the life history of P. jouinae has only been examined in studies on the benthic
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phase of its life cycle (Ramey 2008a, b; Ramey and Bodnar 2008). Temporal patterns of
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abundance and size frequency distributions in Ramey (2008a, b) provided the first details
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regarding the reproductive mode, reproductive period, size at maturity, number of generations in
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a population, and life span. Polygordius spp. are somewhat unusual because two distinct
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planktonic larval forms are exhibited by species within this genus: an exolarva and an endolarva 4
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which differ greatly in their morphology and development. In the exolarva the worm trunk (the
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'body') gradually elongates as new segments form posterior to the hyposphere (Hatschek 1878),
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whereas, in the endolarva developing segments of the trunk of the worm remain folded up inside
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the hyposphere until metamorphosis occurs (Lovén 1843). It is important to note that it was
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Woltereck (1902) who first distinguished between these two larval forms referring to Lovén’s
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North Sea form (endolarva) or Hatschek’s Mediterranean form (exolarva). Prior to this, either
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type of larva was often referred to as Lovén’s larva (as in the case of Fewkes (1883) who clearly
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examined an exolarva), which complicates interpretations of early literature.
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Agassiz (1867) was the first to report exolarvae from the east coast of the United States
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(although he did not know that the larvae belonged to the genus Polygordius) in samples taken at
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Newport, Rhode Island decades before adult Polygordius sp. were found in this area (Stickney
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and Stringer 1957), and more than a century before the first benthic adults were formally
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described from North American coasts (Ramey et al. 2006). Following Agassiz (1867) several
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early studies reported both types of Polygordius spp. larvae from the east coast of the United
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States from Woods Hole, Massachusetts to Beaufort, North Carolina (Fig. 1), (Fewkes 1883;
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Ritter 1892; Bumpus 1898; Cowles 1903). Many early researchers have remarked on the rather
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conspicuous nature of Polygordius spp. in the plankton likely owed to their relatively large size,
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abundance, and high swimming speed (e.g., Fewkes 1883; Ritter1892; Woltereck 1925; present
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study). Videos of swimming behavior of early and late stage P. jouinae exolarvae (referred to as
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Polygordius sp.) collected off coastal New Jersey can be found at
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http://marine.rutgers.edu/~hfuchs/Rutgers_site/Larval_zoo.html (Fuchs 2011).
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These larval forms were present in zooplankton samples collected during the BIOME4 (Bio-physical Interactions in Ocean Margin Ecosystems), (exolarvae only), and COBY (Coastal 5
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Ocean Bio-optical Buoy) cruises in 2006 and 2006-2007, respectively, coordinated by Dr. T.A.
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Moisan, NASA Wallops Flight Facility, which were examined in the present study. Planktonic
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larvae were re-collected in 2010 for molecular analysis. Using a combination of morphological
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and molecular techniques the exolarva was subsequently identified as Polygordius jouinae,
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whereas, the endolarva likely belongs to an undescribed species primarily based on its
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morphology. Samples taken during the BIOME4 cruise examined spatial patterns in distribution
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of P. jouinae exolarvae in three areas along the coast extending from the mouth of Delaware Bay
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to North Carolina (2−6 July, 2006). Temporal patterns of abundance, and size frequency
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distributions of these exolarvae were determined from seasonal samples taken during the COBY
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cruises off Chincoteague, Virginia from January 2006 to December 2007. Among the polychaete
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larvae collected during these cruises, larvae of P. jouinae were numerically abundant; an attribute
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shared by the benthic adult phase. Seasonal trends in abundance of the endolarvae are also
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presented. Light and scanning electron micrography was used to characterize their morphology
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during development.
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Materials and Methods
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Meroplankton sampling
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Sampling was conducted in the southern Mid-Atlantic Bight where the coastal ocean is
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significantly influenced by freshwater inputs from the Delaware and Chesapeake Bays, but
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freshwater inputs are minimal from Chincoteague Bay. Zooplankton samples were collected as
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part of the BIOME4 (Bio-physical Interactions in Ocean Margin Ecosystems) research cruise on
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the R/V Hugh R. Sharp, University of Delaware (2006) and COBY (Coastal Ocean Bio-optical 6
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Buoy) research cruises conducted on the R/V Phillip N. Parker, Chincoteague Bay Field Station,
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formerly The Marine Science Consortium, (2006-2007). These cruises were part of a
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collaboration between researchers from NASA Wallops Flight Facility, NASA Goddard Space
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Flight Center, Marine Science Consortium, and Old Dominion University to characterize and
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monitor biophysical coastal ocean processes in the southern Mid-Atlantic Bight (see Moisan et al.
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2005; Ambler 2008; Ambler et al. 2013). In 2010, additional zooplankton samples were
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collected (as part of the current research) along the COBY transect 2, off Virginia (R/V Philip N.
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Parker, Chincoteague Bay Field Station) to obtain specimens for molecular and morphological
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analysis.
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Southern Mid-Atlantic Spatial Study (BIOME4)
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During the BIOME4 cruise zooplankton samples were collected (July 2−6, 2006) from 28
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stations across the continental shelf along three transects Delaware (n = 12), Chincoteague
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transect 1 (n = 4), and Chesapeake (n = 11), (Table 1, Fig. 2). Each transect included nearshore
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stations at depths 90% of the meroplankton abundance at this station,
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and at one of the offshore Chincoteague (transect 1) stations (Fig. 2b). Exolarvae were present at
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all seven stations sampled nearshore off the mouth of Chesapeake Bay, however, densities of
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exolarvae were relatively higher at nearshore easterly stations (sta. 17−19, 350−1584 ind m-3),
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compared to nearshore southerly stations (sta. 12, 14−16, 62−568 ind m-3) making up 67−95%
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and 13−34% of the meroplankton abundance respectively (Fig. 2a−b). Exolarvae were only
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observed at one station along the Delaware transect (sta. 28, 3.6 ind m-3) making up only 0.53%
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of the meroplankton. Polygodius sp. endolarvae were not observed at any station.
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Seasonal abundance of exo- and endolarvae off Chincoteague (COBY transect 2), 2006−2007
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In 2006 off Chincoteague (COBY transect 2) exolarvae of P. jouinae were first observed on 29
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March (mean = 13.1 ind m-3), (Fig. 4a). Density increased substantially by 13 June (mean = 1,585
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ind m-3), and peaked in the 30 June sample (mean = 3,444 ind m-3). By 12 July, after only 12 d,
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density had declined by 85%, and continued to decline throughout the remainder of the summer
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(August−September). Abundances were significantly lower in 2007 (mean = 1.63 ind m-3)
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compared to 2006 (mean = 255 ind m-3), (χ2 = 13.38, p =
