Mark D. Ohman

Density-dependent mortality in an oceanic copepod population.

Planktonic copepods are primary consumers in the ocean and are perhaps the most numerous metazoans on earth. Secondary production by these zooplankton supports most food webs of the open sea, directly affecting pelagic fish populations and the biological pump of carbon into the deep ocean. Models of marine ecosystems are quite sensitive to the formulation of the term for zooplankton mortality, although there are few data available to constrain mortality rates in such models. Here we present the first evidence for nonlinear, density-dependent mortality rates of open-ocean zooplankton. A high-frequency time series reveals that per capita mortality rates of eggs of Calanus finmarchicus Gunnerus are a function of the abundance of adult females and juveniles. The temporal dynamics of zooplankton populations can be influenced as much by time-dependent mortality rates as by variations in ‘bottom up’ forcing. The functional form and rates chosen for zooplankton mortality in ecosystem models can alter the balance of pelagic ecosystems, modify elemental fluxes into the oceans interior, and modulate interannual variability in pelagic ecosystems.

Analysis of abrupt transitions in ecological systems

The occurrence and causes of abrupt transitions, thresholds, or regime shifts between ecosystem states are of great concern and the likelihood of such transitions is increasing for many ecological systems. General understanding of abrupt transitions has been advanced by theory, but hindered by the lack of a common, accessible, and data-driven approach to characterizing them. We apply such an approach to 30–60 years of data on environmental drivers, biological responses, and associated evidence from pelagic ocean, coastal benthic, polar marine, and semi-arid grassland ecosystems. Our analyses revealed one case in which the response (krill abundance) linearly tracked abrupt changes in the driver (Pacific Decadal Oscillation), but abrupt transitions detected in the three other cases (sea cucumber abundance, penguin abundance, and black grama grass production) exhibited hysteretic relationships with drivers (wave intensity, sea-ice duration, and amounts of monsoonal rainfall, respectively) through a variety of response mechanisms. The use of a common approach across these case studies illustrates that: the utility of leading indicators is often limited and can depend on the abruptness of a transition relative to the lifespan of responsive organisms and observation intervals; information on spatiotemporal context is useful for comparing transitions; and ancillary information from associated experiments and observations aids interpretation of response-driver relationships. The understanding of abrupt transitions offered by this approach provides information that can be used to manage state changes and underscores the utility of long-term observations in multiple sentinel sites across a variety of ecosystems.

Long-term changes in pelagic tunicates of the California Current

Abstract This study analyzes interannual variability in springtime carbon biomass of pelagic tunicates (salps, doliolids, pyrosomes, and appendicularians) over the period 1951–2002 from CalCOFI zooplankton samples taken in the southern sector of the California Current System. The results provide evidence for ecosystem changes between 1976 and 1977 and perhaps between 1998 and 1999. A cool-phase group of salps (Salpa maxima, Pegea socia, Cyclosalpa bakeri, and Cyclosalpa affinis) that was present between 1951 and 1976 was nearly undetectable in Southern California waters during the warm phase of the California Current (1977–98). C. bakeri and C. affinis then re-appeared in 2001. A persistent group of salps (Salpa aspera, Salpa fusiformis, Thalia democratica, Ritteriella picteti, Iasis zonaria) was observed throughout the study period. The cool-phase species tend to be distributed in mid-latitudes, while the distributions of the persistent species extend to equatorial waters. The cool-phase species have been reported to show little evidence of diel vertical migration, while most of the persistent species are reported to be diel migrants. No distinct multi-decadal patterns were observed in the dominant doliolid Dolioletta gegenbauri, but the rarer subtropical doliolid Doliolum denticulatum was present predominantly during the warm phase of the California Current. The recurrence patterns and biogeographic distributions of both salps and doliolids suggest that the warm phase of the California Current was accompanied by at least some intervals of anomalous transport “seeding” organisms from the south. Variations in total pyrosome and total appendicularian carbon biomass are not clearly related to long-term trends in the water column, although the highest pyrosome biomass occurred in earlier decades and appendicularian biomass has increased since 1999. Long-term changes in the biomass of pelagic tunicates appear to be chiefly responsible for the previously documented long-term decline in California Current total zooplankton biomass. The pattern of decline appeared to reverse in 1999, with a shift to cooler temperatures, somewhat reduced thermal stratification, and an increase in biomass of total zooplankton and of pelagic tunicates.

On birth and death in the sea

We present the first comparative study of the stage-specific patterns of mortality of Calanus and Pseudocalanus, two widely distributed genera that are representative of a relatively large-bodied, broadcast spawning calanoid copepod and a relatively small-bodied, egg-brooding calanoid. The study site is Georges Bank, a continental shelf locality in the Northwestern Atlantic with retentive circulation that renders it suitable for studies of population dynamics. Based on extensive mortality estimates from 30 cruises, we find that co-occurring Calanus finmarchicus and Pseudocalanus spp. have markedly different patterns of stage-specific mortality, the former bimodal and the latter relatively uniform with respect to developmental stage. Neither taxon exhibits a monotonic decline in mortality with developmental stage, nor are rates of mortality predictable in a useful manner by copepod body size or by ambient temperature. Young stages of the broadcast-spawning C. finmarchicus show conditional density-dependence of mortality rates, i.e. mortality rates are independent of population density when adult females are low in abundance but positively related to population density at high female abundances. This density-dependence, which is probably attributable to egg cannibalism, introduces a quadratic mortality term into population dynamic models. The egg-brooding Pseudocalanus spp., in contrast, show no evidence of density-dependent mortality. The two taxa illustrate a life history trade-off: the broadcast-spawning Calanus exhibits birth rates that are greatly elevated with respect to those of Pseudocalanus, but there is a compensatory cost in very low survivorship of the freely spawned eggs. Both the high fecundity, high mortality life history of Calanus and the low fecundity, low mortality life history of Pseudocalanus appear to have approximately equal fitness in this study site.

Estimation techniques used in studies of copepod population dynamics — A review of underlying assumptions

Abstract The literature on zooplankton population dynamics provides more estimation techniques than reliable estimates of population parameters. In this review we show how different techniques relate to each other in terms of underlying models and assumptions. There are two main routes to parameter estimates. The vertical approaches utilize the stage-structure of samples taken at the same point in time. They require assumptions about the constancy in the parameters, but relax assumptions concerning advective influence. The horizontal approaches utilize information provided by the stage structure within samples, as well as information on temporal changes in abundance. They relax assumptions about the constancy of parameters, but advective influences may be introduced. Of the horizontal methods, variants of what are commonly termed cohort methods have been widely used. These provide mathematical simplicity, but are based on more restrictive assumptions than methods fitting predescribed models (delay differe...

Differential dormancy of co-occurring copepods

Abstract Four species of planktonic calanoid copepods that co-occur in the California Current System ( Eucalanus californicus Johnson, Rhincalanus nasutus Giesbrecht, Calanus pacificus californicus Brodsky, and Metridia pacifica Brodsky) were investigated for evidence of seasonal dormancy in the San Diego Trough. Indices used to differentiate actively growing from dormant animals included developmental stage structure and vertical distribution; activity of aerobic metabolic enzymes (Citrate Synthase and the Electron Transfer System complex); investment in depot lipids (wax esters and triacylglycerols); in situ grazing activity from gut fluorescence; and egg production rates in simulated in situ conditions. None of the 4 species exhibited a canonical calanoid pattern of winter dormancy – i.e., synchronous developmental arrest as copepodid stage V, descent into deep waters, reduced metabolism, and lack of winter reproduction. Instead, Calanus pacificus californicus has a biphasic life history in this region, with an actively reproducing segment of the population in surface waters overlying a deep dormant segment in winter. Eucalanus californicus is dormant as both adult females and copepodid V’s, although winter females respond relatively rapidly to elevated food and temperature conditions; they begin feeding and producing eggs within 2–3 days. Rhincalanus nasutus appears to enter dormancy as adult females, although the evidence is equivocal. Metridia pacifica shows no evidence of dormancy, with sustained active feeding, diel vertical migration behavior, and elevated activity of metabolic enzymes in December as well as in June. The four species also differ markedly in water content, classes of storage lipids, and specific activity of Citrate Synthase. These results suggest that copepod dormancy traits and structural composition reflect diverse adaptations to regional environmental conditions rather than a uniform, canonical series of traits that remain invariant among taxa and fixed across a species’ range. Such interspecific and regional differences in life history traits need to be incorporated in models simulating Eastern Boundary Current pelagic ecosystem dynamics.

Linking nitrogen dynamics to climate variability off central California: a 51 year record based on 15N/14N in CalCOFI zooplankton

Abstract Long-term variability in zooplankton 15N/14N was investigated in two species of calanoid copepods (Calanus pacificus and Eucalanus californicus) and two chaetognaths (Sagitta bierii and Sagitta euneritica) sampled in the spring of selected years from 1951 to 2001 off the central California coast. No statistically significant trend in 15N/14N was detected for any of the four species, with isotopic ratios in 2001 resembling those in copepods and chaetognaths sampled five decades earlier. Zooplankton body lengths also showed no long-term trends. With respect to proposed regime shifts in this region, heterogeneity in 15N/14N was detected only for S. bierii when comparing the periods 1951–1975, 1978–1998, and 1999–2001. In this species the 15N/14N in the most recent, brief period (1999–2001) averaged slightly lower than in the previous period. Three of the four species (C. pacificus, S. bierii, and S. euneritica) showed significant increases in 15N/14N during major El Ninos. El Nino-related enrichment in 15N could arise as a consequence of increased nitrate demand:supply at the base of the food web or advection of 15N-enriched nitrate from more southerly waters. While a range of physical and climate indices were evaluated, anomalies of 15N/14N from the long-term mean were found to be significantly related only to: (i) the Southern Oscillation Index in the case of both chaetognath species, (ii) a regional surface water temperature record (S. bierii only), (iii) an index of wind-driven coastal upwelling for the surface-dwelling C. pacificus, and (iv) variability in the Pacific Decadal Oscillation for the somewhat deeper-dwelling E. californicus. The relationships among each species’ 15N/14N averaged over the total sampling period was: E. californicus≈C. pacificus⪡S. euneritica

A double-integration hypothesis to explain ocean ecosystem response to climate forcing

Long-term time series of marine ecological indicators often are characterized by large-amplitude state transitions that can persist for decades. Understanding the significance of these variations depends critically on the underlying hypotheses characterizing expected natural variability. Using a linear autoregressive model in combination with long-term zooplankton observations off the California coast, we show that cumulative integrations of white-noise atmospheric forcing can generate marine population responses that are characterized by strong transitions and prolonged apparent state changes. This model provides a baseline hypothesis for explaining ecosystem variability and for interpreting the significance of abrupt responses and climate change signatures in marine ecosystems.

Immunochemical Detection of Predation on Ciliate Protists by Larvae of the Northern Anchovy (Engraulis mordax)

New approaches are needed for investigating planktonic prey-predator interactions in situ, free from enclosures and long term incubations. Lengthy incubations can lead to several artifacts, including selective mortality of planktonic organisms (1) lysis of some taxa upon fixation (2), alteration of prey-predator encounter rates through perturbations of the turbulent flow field (3) and modification of natural search and avoidance behaviors of predators and prey (4). Microscopic analysis of the gut contents of predators is a feasible alternative only if prey leave digestion-resistant hard parts. Here we describe a different approach involving immunochemical methods. We report the development and first application of an immunoassay that permits detection of predation on soft-bodied, nonloricate ciliates (Strombidium sp.). Polyclonal antibodies raised against Strombidium sp. recognize both intact ciliates and partially assimilated ciliate antigens occurring in a predator’s gut. We demonstrate, by both immunochemical and conventional methods, unequivocal predation by first-feeding larvae of the northern anchovy (Engraulis mordax) on nonloricate ciliates. The intensity of the immunochemical reaction, quantified by enzymelinked dot blots and reflection densitometry, is proportional to prey density and to the predator’s ingestion rate. Polyclonal antisera were produced in New Zealand white rabbits (5) against Strombidium sp. cultured on a diet of the bacterium Vibrio natriegens (6). Immunoglobulin G (anti-Strombidium IgG) was isolated from the antiserum by precipitation in 45% (w/v) ammonium sulfate, desalted by gel filtration, then fractionated by diethylaminoethyl ion exchange chromatography. Detailed

OASIS in the sea: Measurement of the acoustic reflectivity of zooplankton with concurrent optical imaging

Abstract A new instrument Optical-Acoustic Submersible Imaging System (OASIS) has been developed for three-dimensional acoustic tracking of zooplankton with concurrent optical imaging to verify the identity of the insonified organisms. OASIS also measures in situ target strengths (TS) of freely swimming zooplankton and nekton of known identity and 3-D orientation. The system consists of a three-dimensional acoustic imaging system (FishTV), a sensitive optical CCD camera with red-filtered strobe illumination, and ancillary oceanographic sensors. The sonar triggers the acquisition of an optical image when it detects the presence of a significant target in the precise location where the camera, strobe and sonar are co-registered. Acoustic TS can then be related to the optical image, which permits identification of the animal and its 3-D aspect. The system was recently deployed (August 1996) in Saanich Inlet, B.C., Canada. Motile zooplankton and nekton were imaged with no evidence of reaction to or avoidance of the OASIS instrument package. Target strengths of many acoustic reflectors were recorded in parallel with the optical images, triggered by the presence of an animal in the correct location of the sonar system. Inspection of the optical images, corroborated with zooplankton sampling with a MOCNESS net, revealed that the joint optically and acoustically sensed taxa at the site were the euphausiid Euphausia pacifica, the gammarid amphipod Orchomene obtusa, and a gadid fish. The simultaneous optical and acoustic images permitted an exact correlation of TS and taxa. Computer simulations from a model of the backscattered strength from euphausiids are in good agreement with the observed data.