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The Ctenophore Mnemiopsis in Native and Exotic Habitats: U.S. Estuaries Versus the Black Sea Basin

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The Ctenophore Mnemiopsis in Native and Exotic Habitats: U.S. Estuaries Versus the Black Sea Basin Hydrobiologia 451: 145–176, 2001. 145 © 2001 Kluwer Academic Publishers. Printed in the Netherlands. The ctenophore Mnemiopsis in native and exotic habitats: U.S. estuaries versus the Black Sea basin Jennifer E. Purcell1,2, Tamara A. Shiganova3, Mary Beth Decker1,4 & Edward D. Houde5 1University of Maryland Center for Environmental Science, Horn Point Laboratory, P.O. Box 775, Cambridge, MD 21613, U.S.A. 2Present address: Shannon Point Marine Center, 1900 Shannon Point Rd., Anacortes, WA 98221, U.S.A. E-mail: [email protected] 3P.P. Shirshov Institute of Oceanology, Russian Academy of Sciences, 36 Nakhimovskiy Pr., Moscow 117851, Russia 4Present address: Dept. of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520, U.S.A. 5University of Maryland Center for Environmental Science, Chesapeake Biological Laboratory, P.O. Box 38, Solomons, MD 20688-0038, U.S.A. Key words: Beroe, Chesapeake Bay, fish, jellyfish, predation, zooplankton Abstract The native habitats of the ctenophore, Mnemiopsis, are temperate to subtropical estuaries along the Atlantic coast of North and South America, where it is found in an extremely wide range of environmental conditions (winter low and summer high temperatures of 2 and 32 ◦C, respectively, and salinities of <2–38). In the early 1980s, it was accidentally introduced to the Black Sea, where it flourished and expanded into the Azov, Marmara, Mediterranean and Caspian Seas. We compile data showing that Mnemiopsis has high potentials of growth, reproduction and feeding that enable this species to be a predominant zooplanktivore in a wide variety of habitats; review the population distributions and dynamics of Mnemiopsis in U.S. waters and in the Black Sea region; and examine the effects of temperature and salinity, zooplankton availability and predator abundance on Mnemiopsis population size in both regions, and the effects of Mnemiopsis on zooplankton, ichthyoplankton and fish populations, focusing on Chesapeake Bay and the Black Sea. In both regions, Mnemiopsis populations are restricted by low winter tem- peratures (<2 ◦C). In native habitats, predators of Mnemiopsis often limit their populations, and zooplanktivorous fish are abundant and may compete with the ctenophores for food. By contrast, in the Black Sea region, no obvious predators of Mnemiopsis were present during the decade following introduction when the ctenophore populations flourished. Additionally, zooplanktivorous fish populations had been severely reduced by over fishing prior to the ctenophore outbreak. Thus, small populations of potential predators and competitors for food enabled Mnemiopsis populations to swell in the new habitats. In Chesapeake Bay, Mnemiopsis consumes substantial proportions of zooplankton daily, but may only noticeably reduce zooplankton populations when predators of Mnemiopsis are uncommon. Mnemiopsis also is an important predator of fish eggs in both locations. In the Black Sea, reductions in zooplankton, ichthyoplankton and zooplanktivorous fish populations have been attributed to Mnemiopsis.We conclude that the enormous impact of Mnemiopsis on the Black Sea ecosystem occurred because of the shortage of predators and competitors in the late 1980s and early 1990s. The appearance of the ctenophore, Beroe ovata,may promote the recovery of the Black Sea ecosystem from the effects of the Mnemiopsis invasion. Introduction world’s oceans. In estuarine and coastal waters, cten- ophores can reach great abundances. They feed at Comb jellies comprise a diverse phylum (Ctenophora) high rates on zooplankton and ichthyoplankton, and of delicate, gelatinous species living throughout the thereby may be detrimental to fish populations. They 146 are well adapted for rapid population growth, having Black Sea, which are at the same latitude, have sim- high rates of feeding, growth and reproduction. ilar ranges of environmental conditions, and similar The native habitats of ctenophores in the genus zooplankton and zooplanktivorous fish assemblages. Mnemiopsis are estuaries along the eastern coastline of North and South America. Mnemiopsis is probably the most-studied ctenophore genus in the world because of Body composition, metabolism, growth and its great abundance in estuaries in heavily populated reproduction of Mnemiopsis areas of the U.S., and because of its explosive pop- ulation growth after accidental introduction into the Body composition Black Sea in the early 1980s. It has spread from the Black Sea to the Seas of Azov, Marmara and eastern The relationships among various measures of body Mediterranean, and in 1999, it appeared for the first size of Mnemiopsis may vary with ctenophore size, sa- time in the Caspian Sea. At present, its impact is a linity and feeding history (Table 1). Oral-aboral length serious problem for the ecosystems of these basins. measurements are somewhat subjective due to the The identities of species within the genus Mne- flaccid body, as illustrated by the variation in length- miopsis are uncertain. Two species names have been to-wet weight conversions (Table 1). Biovolume (V commonly used, M. leidyi A. Agassiz, which has in ml) typically is measured in field studies and is been used for areas above Cape Hatteras in the U.S., roughly equivalent to wet weight (WW in g). Live and M. mccradyi Mayer, 1900, which has been used WW can be calculated from tentacle bulb length below Cape Hatteras (Larson, 1988), and both spe- in formalin-preserved samples (Purcell, 1988). Dry cies are listed from South America (Mianzan, 1999). weight (DW) commonly is measured, but results dif- Mayer (1912) considered the high body density and fer depending on the salt content of the ctenophore, the warts on the body surface to be specific fea- which reflects ambient salinity. Carbon (C) and ni- tures of M. mccradyi, however, these features were trogen (N) contents as percent of DW vary, generally formerly noted in M. leidyi (in A. Agassiz, 1865; being inversely related to ctenophore size and directly Fewkes, 1881). Recent investigations reveal indistin- related to prey density (Reeve et al., 1989; Borodkin guishable specimens from North and South America & Korzhikova, 1991). C%DW ranged from 13.1% in (K. Bayha, pers. comm.). Experimental results on 1.1 mm ctenophores to 1.5% in 20 mm specimens. respiration, excretion, egg production, feeding and C%DW ranged from 1% when fed at ≤20 prey l−1 to growth on Mnemiopsis from northern and southern 2% at 200 prey l−1. Chemical composition (glycogen, U.S. are indistinguishable (Kremer, 1994). mono- and polysaccharides) of Mnemiopsis has been Identification of the ctenophore that appeared in further studied by Anninsky et al. (1998). the Black Sea was confused by inconsistencies in description of morphological features of the genus Metabolism Mnemiopsis by its first researchers. The introduced ctenophore was called both M. leidyi and M. mccradyi More extensive research has been conducted on the (e.g. Vinogradov et al., 1989; Zaika & Sergeeva, respiration and excretion of Mnemiopsis than on any 1990). Seravin (1994) revised the genus Mnemiopsis, other gelatinous species. The average respiratory quo- concluding that it includes only one polymorphic spe- tient (molecular ratio) of CO2:O2 of 0.74 and O2:NH4 cies, M. leidyi. Due to the uncertainty of clear species, of 6.7 (O:N atomic ratio = 13.3) are indicative of we will refer to the ctenophores by the genus name. protein and lipid metabolism, and suggest that Mne- In this review, we explore the effects of the en- miopsis are strict carnivores (Kremer, 1977). Weight- vironment on populations of Mnemiopsis.First,we specific metabolism of Mnemiopsis and other cten- consider how temperature, salinity and prey densit- ophores has been reported to depend on body size ies affect the ctenophore’s composition, metabolism, (Miller, 1970; Nemazie et al., 1993) (Table 2), how- individual growth and reproduction. Then, we exam- ever, Kremer (1975a, 1977, 1982) found no weight- ine the conditions found in the habitats of Mnemiopsis specific effects. Total nitrogen excretion is comprised + and how their populations vary with physical and bio- of 66% NH4 and 34% dissolved organic nitrogen logical factors, first considering native habitats and (Kremer, 1977, 1982). Ammonium excretion rates then exotic habitats. We have chosen to concentrate per g DW reported from Chesapeake Bay are 3-fold on comparisons between the Chesapeake Bay and the higher than for Narragansett Bay, but are similar when 147 Table 1. Biometric conversions for Mnemiopsis. V = live volume in ml, L = total length in mm, WW = wet weight in g, DW = dry weight in g, C = carbon in mg, N = nitrogen in mg Conversion Salinity Source WW = 1.017V - 0.122 31 Kremer & Nixon (1976) WW = 0.009L1.872 31 Kremer & Nixon (1976) WW=0.00236L2.35 18 Vinogradov et al. (1989) WW=0.00079 L2.51 18 Pavlova & Minkina (1993) WW= 0.001074L2.76 — Finenko et al. (1995) WW=0.0023L2.05, R=0.94 (Spring) 18 Shiganova (unpublished) WW=0.0061L1.81, R=0.95 (Summer) 18 Shiganova (unpublished) DW = 0.034WW 31 Kremer & Nixon (1976) DW=0.0331WW0.939 18 Tzikhon-Lukanina & Reznichenko (1991) DW = 0.0095WW - 0.0014 6–12 Nemazie et al. (1993) C = 0.0005V 6–12 calculated from Nemazie et al. (1993) C%WW=0.00012% 18 Vinogradov et al. (1989) C%DW = 1.7% 31 Kremer & Nixon (1976) C% DW = 4.2% 18 Finenko et al. (1995) C%DW = 5.1% 6–12 Nemazie et al. (1993) N% DW = 0.5% 31 Kremer (1976) N%DW = 1.3% 6–12 Nemazie et al. (1993) + −1 −1 −1 −1 Table 2. Metabolic rates of Mnemiopsis. Excretion (E) in µgatomsNH4 -N g DW h . Respiration (R) in µgatomsO2 gDW h ,R1 −1 −1 −1 −1 −1 −1 ◦ ∗ in ml O2 ind h ,R2 in µlO2 gDW h ,R3 in µlO2 ind h . T = temperature in C, DW = g dry weight. = calculated from the ◦ equations for ctenophores 0.4 g DW at 22 C, and using the conversions 1 ml O2 =1.42mgO2 = 44.88 µmol O2 = 89.76 µgatomsO2 Rate equation Temperature Salinity R or E at Source ◦ ◦ ( C) 22 C,0.4gDW − − ∗ (µgatomsgDW 1 h 1) E = 0.059 e0.13T 10–24 31 1.03 Kremer (1975b) E = 1.952 DW0.742 18–28 6–12 1.17 Nemazie et al.
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