Stephen M. Bollens

Zooplankton invasions: a brief review, plus two case studies from the northeast Pacific Ocean

Invasions of aquatic habitats by non-indigenous species (NIS), including zooplankton, are occurring at an alarming rate and are causing global concern. Although hundreds of such invasions have now been documented, surprisingly little is known about the basic biology and ecology of these invaders in their new habitats. Here we provide an overview of the published literature on NIS zooplankton, separated by life history (holoplankton vs. meroplankton), habitat (marine, estuarine, freshwater), and biological level of organization or topic (e.g. distribution and range extension, physiology, behavior, feeding, community impacts, ecosystem dynamics, etc). Amongst the many findings generated by our literature search, perhaps the most striking is the paucity of studies on community and ecosystem level impacts of NIS zooplankton, especially in marine and estuarine systems. We also present some results from two ongoing studies of invasive zooplankton in the northeast Pacific Ocean – Pseudodiaptomus inopinus in Washington and Oregon coastal estuaries, and Tortanus dextrilobatus in San Francisco Bay. Both of these Asian copepods have recently expanded their range and can at times be extremely abundant (103 m−3). We also examine some aspects of the trophic (predator–prey) ecology of these two invasive copepods, and find that they are likely to be important in the flow of material and energy in the systems in which they now pervade, although their impacts at the ecosystem level remain to be quantified. Finally, the findings of both our literature search and our two case studies of invasive zooplankton lead us to make several recommendations for future research.

Diel vertical migration in zooplankton: field evidence in support of the predator avoidance hypothesis

We report results of a field test of the predator avoidance hypothesis as an explanation of the adaptive significance of diel vertical migration in zooplankton. We determined the vertical distribution and diel migration of the planktonic copepod Acartia hudsonica, concurrently with the abundance of pelagic fish, transparency and thermal stratification of the water column, on six cruises over a one year period in a temperate marine lagoon (Jakles Lagoon, San Juan Island, Washington, USA). Striking seasonal variability was observed in all biological and environmental variables. Linear regressions of the strength of diel vertical migration in A. hudsonica on these environmental variables resulted in only one statistically significant relationship, that between copepod diel vertical migration and predator abundance. These results, together with those of previous studies, point to diel vertical migration as a widespread behavioral response of planktonic prey to the presence of their predators.

Recruitment, growth, and diel vertical migration of Euphausia pacifica in a temperate fjord

The pelagic crustacean Euphausia pacifica Hansen was sampled with a multiple-sample 1.0 m2 Tucker trawl and a multiple-sample 1.0 m2 vertical net in Dabob Bay, Washington on 17 dates between May 1985 and October 1987. Size (stage) structure and abundance of the population were determined for each date, while vertical distribution and diel migration were determined for 13 dates. Although internannual variability in both timing and magnitude of events occurred, consistent patterns were discernable. The population produced a large pulse of larvae (2 to 5 mm) in late spring of each year, apparently in response to the vernal phytoplankton bloom. Much lower abundances of larvae occurred during summer and autumn of each year, and larvae were completely absent during winter. Recruitment to the juvenile (6 to 9 mm) and adult (≥10 mm) stages was strongest during the summer, with abundances of these individuals peaking in summer and autumn. Individual growth rates, determined by modal progression analysis, were calculated for E. pacifica. Rates ranged from zero for some adult cohorts during the winter to 0.12 mm d-1 for larvae during spring. The latter are among the highest ever reported for this species in the field. The vertical distributions and diel vertical migrations (DVM) of E. pacifica varied seasonally and between size (stage) classes. At night, all size classes were distributed in the surface layer (upper 25 m) irrespective of season or year. During the day, the larger/older stages were always distributed at middepths (50 to 125 m). In contrast, the daytime distribution of the larvae was more variable, being concentrated at the surface during spring and early summer of 1985, and at increasing depths later in the summer and autumn of 1985 and again in spring of 1986. This resulted in invariant DVM in the juveniles and adults, but variable DVM in the larvae, the latter of which is hypothesized to be a response to variable abundances of zooplanktivorous fish.

The effects of haloclines on the vertical distribution and migration of zooplankton

Abstract While the influence of horizontal salinity gradients on the distribution and abundance of planktonic organisms in estuaries is relatively well known, the effects of vertical salinity gradients (haloclines) are less well understood. Because biological, chemical, and physical conditions can vary between different salinity strata, an understanding of the behavioral response of zooplankton to haloclines is crucial to understanding the population biology and ecology of these organisms. We studied four San Francisco Bay copepods, Acartia ( Acartiura ) spp., Acartia ( Acanthacartia ) spp., Oithona davisae , and Tortanus dextrilobatus , and one species of larval fish ( Clupea pallasi ), in an attempt to understand how and why zooplankton respond to haloclines. Controlled laboratory experiments involved placing several individuals of each species in two 2-m-high tanks, one containing a halocline (magnitude varied between 1.4 and 10.0 psu) and the other without a halocline, and recording the location of each organism once every hour for 2–4 days using an automated video microscopy system. Results indicated that most zooplankton changed their vertical distribution and/or migration in response to haloclines. For the smaller taxa ( Acartiura spp., Acanthacartia spp., and O. davisae ), this behavior took the form of accumulating in or below the halocline, while the effects on the larger species ( C. pallasi and T. dextrilobatus ) were more subtle. C. pallasi yolk sac and 3- to 6-day-old larvae seemed to pause or remain in the halocline during their diel migration, while 14- to 17-day-old larvae appeared to avoid the halocline by remaining in deeper, more saline water. There were very few statistically significant effects of haloclines on the vertical distribution of T. dextrilobatus . Subsequent mortality experiments with Acartiura spp., Acanthacartia spp. and T. dextrilobatus indicated that the behavioral changes seen in the halocline studies were not associated with any salinity-induced mortality per se, although more subtle affects of physiological stress could not be ruled out. These results point to a high degree of flexibility in vertical migration behavior within a given species as well as large variation between species. Such behavioral flexibility is likely to be very important in allowing planktonic organisms generally, and estuarine organisms in particular, to maintain or alter position relative to currents, food, and predators.

Voracious planktonic hydroids: unexpected predatory impact on a coastal marine ecosystem

Abstract-Hydroids are typically attached, benthic cnidarians that feed on a variety of small prey. During sampling on Georges Bank in spring 1994, we found huge numbers of hydroids suspended in the plankton. They fed on young stages of copepods that are an important prey for fish, as well as on young fish themselves. Two independent methods were used to estimate feeding rates of the hydroids; both indicate that the hydroids are capable of consuming from 50% to over 100% of the daily production of young copepods. These results suggest that hydroids can have a profound effect on the population dynamics of zooplankton and young fish on Georges Bank. Copyright 0 1996 Elsevier Science Ltd INTRODUCTION The life history of marine hydrozoans (Phylum Cnidaria) is typically an alternation between a sessile hydroid phase and a motile medusa. The hydroids form colonies attached to seaweed, rocks or other organisms, and their feeding polyps (hydranths) prey on small organisms, eggs and detrital matter. The medusae are usually released to feed and disperse in the plankton (Hyman, 1940). We report observations from Georges Bank on the occurrence of suspended colony fragments of the hydroid

UV light and vertical distribution of the marine planktonic copepod Acartia hudsonica Pinhey

Abstract Of the many hypotheses put forth to explain the possible adaptive value of daytime residence in subsurface waters and diel vertical migration behavior of Zooplankton, avoidance of potentially harmful UV radiation has only recently been proposed. We undertook a manipulative field experiment to test the effect of UV-B (290–315 nm) solar radiation on the daytime vertical distribution of the marine planktonic copepod Acartia hudsonica Pinhey. Since no statistically significant difference in the daytime depth distributions of adult A. hudsonica in control and UV-B-filtered treatments was found, we conclude that some other factor(s) must determine the daytime vertical distribution of this copepod.

Environmental influence on cyanobacteria abundance and microcystin toxin production in a shallow temperate lake.

The increasing frequency of harmful cyanobacterial blooms in freshwater systems is a commonly recognized problem due to detrimental effects on water quality. Vancouver Lake, a shallow, tidally influenced lake in the flood plain of the Columbia River within the city of Vancouver, WA, USA, has experienced numerous summertime cyanobacterial blooms, dominated by Aphanizomenon sp. and Anabaena sp. Cyanobacteria abundance and toxin (microcystin) levels have been monitored in this popular urban lake for several years; however, no previous studies have identified which cyanobacteria species produce toxins, nor analyzed how changes in environmental variables contribute to the fluctuations in toxic cyanobacteria populations. We used a suite of molecular techniques to analyze water samples from Vancouver Lake over two summer bloom cycles (2009 and 2010). Both intracellular and extracellular microcystin concentrations were measured using an ELISA kit. Intracellular microcystin concentrations exceeded WHO guidelines for recreational waters several times throughout the sampling period. PCR results demonstrated that Microcystis sp. was the sole microcystin-producing cyanobacteria species present in Vancouver Lake, although Microcystis sp. was rarely detected in microscopical counts. qPCR results indicated that the majority of the Microcystis sp. population contained the toxin-producing gene (mcyE), although Microcystis sp. abundance rarely exceeded 1 percent of overall cyanobacteria abundance. Non-metric multidimensional scaling (NMDS) revealed that PO4-P was the main environmental variable influencing the abundance of toxic and non-toxic cyanobacteria, as well as intracellular microcystin concentrations. Our study underscores the importance of using molecular genetic techniques, in addition to traditional microscopy, to assess the importance of less conspicuous species in the dynamics of harmful algal blooms.

Feeding dynamics of the copepod Diacyclops thomasi before, during and following filamentous cyanobacteria blooms in a large, shallow temperate lake

Cyanobacteria blooms are an increasing problem in temperate freshwater lakes, leading to reduced water quality and in some cases harmful effects from toxic cyanobacteria species. To better understand the role of zooplankton in modulating cyanobacteria blooms, from 2008 to 2010 we measured water quality and plankton abundance, and measured feeding rates and prey selectivity of the copepod Diacyclops thomasi before, during and following summertime cyanobacteria blooms in a shallow, eutrophic lake (Vancouver Lake, Washington, USA). We used a combined field and experimental approach to specifically test the hypothesis that copepod grazing was a significant factor in establishing the timing of cyanobacteria bloom initiation and eventual decline in Vancouver Lake. There was a consistent annual succession of zooplankton taxa, with cyclopoid copepods (D. thomasi) dominant in spring, followed by small cladocerans (Eubosmina sp.). Before each cyanobacteria bloom, large cladocerans (Daphnia retrocurva, Daphnia laevis) peaked in abundance but quickly disappeared, followed by brief increases in rotifers. During the cyanobacteria blooms, D. thomasi was again dominant, with small cladocerans abundant in autumn. Before the cyanobacteria blooms, D. thomasi substantially consumed ciliates and dinoflagellates (up to 100% of prey biomass per day), which likely allowed diatoms to flourish. A shift in copepod grazing toward diatoms before the blooms may have then helped to facilitate the rapid increase in cyanobacteria. Copepod grazing impact was the highest during the cyanobacteria blooms both years, but focused on non-cyanobacteria prey; copepod grazing was minimal as the cyanobacteria blooms waned. We conclude that cyclopoid copepods may have an indirect role (via trophic cascades) in modulating cyanobacteria bloom initiation, but do not directly contribute to cyanobacteria bloom decline.

Amphipods on a deep-sea hydrothermal treadmill

Abstract Conspicuous swarms of a pardaliscid amphipod were observed at about 2520 and 2580 m depth in the East Pacific Rise vent field during dives with the submersible Alvin . Swarms occurred in association with mussels, clams and tubeworms, and were located above, and immediately downstream of cracks with emanating hydrothermal water. Numerical density sometimes exceeded 1000 individuals 1 −1 , which is 3 orders of magnitude greater than any previous report on pelagic crustaceans from the deep sea. The amphipods, however, were not obligatory swarmers, and thin-layered shoals and scattered individuals were observed. Orientation of individuals was often polarized as they headed into the venting flow, swimming vigorously at 5–10 cm s −1 to maintain their position in the current. Retention within the preferred habitat requires an average swimming speed corresponding to the average current speed, suggesting a sustained swimming of > 10 body lengths s −1 . These observations contrast with the general concept of low swimming activity in deep-sea crustaceans.

Fish assemblages across a vegetation gradient in a restoring tidal freshwater wetland: diets and potential for resource competition

Marsh habitats have been the focus of recent worldwide restoration efforts due to their degradation and destruction as a result of human development. We assessed fish resource use at a naturally restoring marsh (Liberty Island, California, USA) by comparing diet composition, stomach fullness, normalized stomach weight, and diet overlap across a vegetation gradient. Fish were collected using gill nets and fyke nets at six sites during spring 2010, summer 2011 and winter 2012. We analyzed 392 stomachs from the eleven most abundant species collected. Prey composition and biomass varied seasonally for all fish species, but there were no notable differences across sites or seasons for stomach fullness or normalized stomach weight for most fish species. Results from non-metric multidimensional scaling (NMDS) and two-way analysis of similarities (ANOSIM) indicated minimal diet overlap between species (R = 0.633, p = 0.001) and seasons (R = 0.413, p = 0.001). Seasonal habitat and resource use across the vegetation gradient was species-specific. Small but significant spatial diet differences were detected for inland silverside, striped bass and bigscale logperch. Delta smelt exhibited seasonal diet differences by shifting from chironomids and zooplankton during spring, to amphipods and zooplankton during winter. More generally, fish maintained stomach fullness across all sites and seasons while maintaining minimal dietary overlap. Our study emphasizes the importance of tidal marshes as feeding habitat for several fish species, including the endangered delta smelt.