Previous descriptions have noted that the stomach samples of spiny dogfish,
There have been several documented instances of gelatinous zooplankton blooms for a wide range of marine ecosystems. Both enclosed (e.g., Black Sea, Caspian Sea, Sea of Azov, and Sea of Marmara) and relatively enclosed/semiopen (e.g., Adriatic Sea, Baltic Sea, Gulf of Mexico, Bering Sea, and Mediterranean Sea) marine ecosystems have exhibited these blooms [
Additionally, sampling gelatinous zooplankton remains a major challenge for biological oceanography [
In a prior study [
Map of the study area, the Northeast U.S. (NEUS) continental shelf. Common regions of Gulf of Maine (GM), Georges Bank (GB), Southern New England (SNE), and Middle Atlantic Bight (MAB) are highlighted.
In our prior study [
The broad-scale, long-term sampling program of stomach contents of fishes from the Northeast U.S. continental shelf ecosystem (Figure
Although the program started in 1963, we focused on our study on spiny dogfish stomachs (
Ctenophora were readily identifiable in the stomachs of spiny dogfish, at sea upon macroscopic inspection, by their obvious firm-gelatin constitution, small and clear ball-like shape, uniquely (relative to any other spiny dogfish prey) colored pinkish-gray masses, and particularly the ctene rows. Stomach contents identified as Ctenophora could have been
The traditional method for monitoring zooplankton levels in the Northeast U.S. shelf ecosystem has been plankton nets. However, plankton net surveys from 1977 to the present only record a very small number of observations of ctenophores (less than 2% of all tows taken). When compared with direct methods of sampling gelatinous zooplankton in the marine environment (e.g., nets), stomach sampling methods largely eliminated concerns of specimens breaking apart and becoming unidentifiable and/or indistinguishable [
The significance of ctenophores in the diet of spiny dogfish was explored in terms of consumption, energy density, and diet composition (percentage of weight) relative to other prey types. The caloric value of ctenophores is estimated to be between 90 and 200 cal g−1 wet weight (1 cal = 4.1868 J) [
Energy density for common spiny dogfish (
Prey | kJ/g | Reference |
---|---|---|
Ctenophores—lower | 0.38 | [ |
Ctenophores—upper | 0.84 | [ |
|
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shrimp—lower | 4.88 | [ |
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shrimp—upper | 9.52 | [ |
Amphipods | 9.67 | [ |
General | ||
invertebrates—lower | 1.00 | [ |
General | ||
invertebrates—upper | 10.0 | [ |
Medusae | 0.25 | [ |
Ctenophores | 0.21 | [ |
Cephalopods | 5.50 | [ |
Bivalves | 1.54 | [ |
Gastropods | 2.28 | [ |
Zooplankton | 1.64 | [ |
General | ||
crustaceans—lower | 3.50 | [ |
General | ||
crustaceans—upper | 5.40 | [ |
Tunicates | 0.40 | [ |
Fish—lower | 4.00 | [ |
Fish—upper | 7.00 | [ |
Forage fish—lower | 10.0 | [ |
|
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Forage fish—upper | 20.0 | [ |
The energetic contribution of common prey items for spiny dogfish, including ctenophores, was estimated by using a simple product of percent diet composition, energy density, and mean amount of total food consumed. Additionally, we made calculations that also included the digestion rate of the prey item to estimate the energetic contribution of common prey items while accounting for the different digestion rates of prey body types.
To place bounds on the estimates of potential abundance and biomass of ctenophores in the Northeast U.S. shelf ecosystem, we employed five calculation methodologies. The estimates here refer to biomass over the total area of the Northeast U.S. shelf ecosystem (230,000 km2). The five methodologies were a digestion time approach, a consumption model approach, simple frequency of occurrence, a swept volume model, and a plankton net method.
Biomass of ctenophores within the whole of the NEUS was estimated using the mass of ctenophores in the stomachs of spiny dogfish and the estimated digestion time of ctenophores within spiny dogfish. The mass of ctenophores per year (
The biomass of ctenophores on the shelf was also estimated using a consumption model method [
To scale to an annual, total estimate,
A simple method of estimating the biomass of ctenophores was used to estimate ctenophore biomass (
The swept volume of a dogfish was defined as the product of the gape area and the time and distance a dogfish swims per day. We assumed a gape width of 3 cm, 22 hours of feeding in a day, and a swimming velocity of 1 m s−1. Observations of spiny dogfish morphology and swimming behavior were used to conservatively estimate gape width and swimming speed. The feeding time estimate was made to allow some time spent on nonfeeding activities (2 hours). Using the gape width as a diameter and scaled to the daily distance swum (product of speed and swimming time), the resulting swept volume
Prior ctenophore abundance estimates for the NEUS shelf were estimated directly, system-wide, as part of the Energy Modeling and Analysis Exercise (EMAX) [
The energy density (KJ g−1) of common spiny dogfish prey, including ctenophores, indicated that herring and mackerel had the highest energy density, whereas ctenophores had the lowest energy density (Table
Energy density of selected common prey types scaled by diet composition.
When digestion time was factored into the scaled energy density calculations, the relative significance of ctenophores increased. Under the lowest digestion time, ctenophores contributed as much energy to the diet of spiny dogfish as mackerel but were still much lower than other fishes (Figure
Energy density of common prey items scaled for diet composition and digestion time.
Considering a range of possible digestion times for ctenophores in dogfish, the mean estimated number of ctenophores in this continental shelf ecosystem ranged from 8.1 × 1013 at the fastest digestion time of 0.25 h to 8.5 × 1011 at the slowest digestion time of 24 h (Figure
Estimated number of ctenophores as a function of ctenophore digestion time (h) for minimum, maximum, and average dogfish abundance estimates.
Considering a range of digestibility coefficients (
Estimated number of ctenophores as a function of digestibility coefficient (
When using the simple frequency of occurrence method, the mean number of ctenophores was 1.6 × 108, ranging from 3.7 × 107 to 1.3 × 109, using the minimum and maximum estimates of dogfish abundance (Figure
Estimates of ctenophore abundance using the simple frequency of occurrence in dogfish method. Results presented for minimum, maximum, and average dogfish abundance estimates.
There were an estimated 1.2 × 1010 ctenophores per year in the entire continental shelf ecosystem using the swept volume method. The estimate of ctenophore biomass was 4.2 thousand MT from this method.
Using the plankton net and associated methodology described in EMAX, there were approximately 8.3 × 1013 ctenophores in the entire continental shelf ecosystem. This estimate was derived from the average ctenophore concentration (10 m−2) of 22, 88, 20, and 6 for the Middle Atlantic Bight, Southern New England, Georges Bank, and Gulf of Maine regions, respectively. The estimate of total ctenophore biomass was approximately 30,000 thousand MT.
Overall, the five methods for determining the abundance of ctenophores spanned six orders of magnitude, with mean values ranging between 108 and 1013 (Figure
Average number (a) and average biomass (b) of ctenophores (1000 MT) as estimated from the different methods.
Ctenophores have a low energy density relative to other spiny dogfish prey such as mackerel, herring, shrimp, and squid. When the energy densities of individual prey items are scaled by diet composition, small pelagic fishes become the most energetically dominant component of the spiny dogfish diet.
Our results do indicate that faster digestion times for gelatinous zooplankton can increase the energetic importance of ctenophores in dogfish. We calculated the diet-scaled energetic importance (energy density) of ctenophores for a range of digestion rates from 0.25 h to 24 h. Our estimates indicate more than a fivefold difference in energy contributed by ctenophores when digestion times range from even just 0.75 to 4 h. This range of digestion times is shorter than other common prey items like mackerel. While we do not have empirical data for the digestion time of ctenophores in spiny dogfish, we do have empirically derived digestion rates of a tentaculate ctenophore
We infer from these results that spiny dogfish feed on ctenophores in an opportunistic feeding mode, eating them as encountered while swimming in the water column. This implies that spiny dogfish neither select for nor avoid ctenophores. It may be that ctenophores serve as a supplementary food source allowing spiny dogfish to maintain some basic energy demands, but it is unlikely that spiny dogfish glean a large portion of their bioenergetic demands solely from ctenophores. We suspect that this is generally true for other fishes that prey upon gelatinous zooplankton, with a few exceptions (e.g., Stromateid fishes such as
Our model analyses and assumptions imply a level of uncertainty in amount of ctenophores consumed by spiny dogfish in the NEUS on the range of six orders of magnitude. Abundance estimates were on the order of 108 to 1013 individuals in the NEUS. Estimates for biomass were similarly quite widespread, roughly ranging between 101 and 105 thousand MT. These estimates are quite variable and encompass quite a large range but do provide a reasonable bound of possible estimates of ctenophore abundance. This work in many ways represents a rudimentary sensitivity analysis among different methods and serves to provide a bound about the true ctenophore abundance, outside of which most estimates are likely to be ecologically unfeasible.
Some key assumptions in the different methods we used all merit further investigation. Chief among them is the identification of major unknowns: digestion time, ctenophore weight, and true abundance of “sampler” fish. Obviously, there is a tradeoff among the methods used in terms of data or parameter requirements and simplicity. That most of our estimates provided values of similar orders of magnitude adds confidence to the range of estimates presented.
Furthermore, a recent study from Narragansett Bay, Rhode Island, USA, reported concentrations of ctenophores between 0.1 m−3 and 1000 m−3 [
Ctenophora and other gelatinous zooplankton are inherently difficult to sample and survey, particularly at synoptic temporal and spatial scales [
The spiny dogfish appears to be a good sampler for ctenophores that can support studies like this one. Previous studies [
The amount of gelatinous zooplankton in the world’s oceans remains a major question. The examples from other ecosystems (e.g., [
The authors declare that there is no conflict of interests regarding the publication of this paper.
The authors thank the numerous staff at the NEFSC, past and present, who have collected fish stomachs on the routine surveys. They also thank two anonymous reviewers for their constructive comments on earlier drafts of this paper.