Costello, J. H.,et al. Seasonal refugia, shoreward thermal …fox.rwu.edu/jellies/references/costello et al 2006 (LO... · 2012. 2. 23. · 1820 Costello et al. 79.0 m3, depending

Seasonal refugia, shoreward thermal amplification, and metapopulation dynamics of the

ctenophore Mnemiopsis leidyi in Narragansett Bay, Rhode Island

J. H. Costello1

Biology Department, Providence College, Providence, Rhode Island 02918

B. K. Sullivan, D. J. Gifford, D. Van Keuren, and L. J. SullivanGraduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island 02882

Abstract

The lobate ctenophore Mnemiopsis leidyi occurs throughout Narragansett Bay, Rhode Island, during warmsummer months but is often undetectable in the central portion of the bay during winter months. During 2 yr ofweekly sampling, we found that M. leidyi populations in a shallow embayment, Greenwich Cove, eitheroverwintered or were only briefly absent during winter. The Greenwich Cove population reproduced weeks earlierand reached higher average and peak population concentrations than open-bay populations. Shallow embaymentpopulations such as that in Greenwich Cove probably serve as source populations that inoculate the main regionof the bay by advective transport in the spring months. We propose that earlier occurrences of M. leidyi duringrecent years are due to amplification of pulsed spring warming events that permit early reproduction in theshallow embayments that serve as source regions for M. leidyi in Narragansett Bay. We further suggest that thesource-sink perspective we describe is relevant not only to Narragansett Bay but other temperate regions of theworld persistently occupied by M. leidyi.

The importance of Mnemiopsis leidyi as a planktonicpredator has been documented by a large body of researchon its feeding capabilities (Kremer 1975; Reeve et al. 1978;Waggett and Costello 1999) and trophic impacts (Kremer1979; Shiganova et al. 2001; Sullivan et al. 2001). Thesepredatory capabilities underlie the importance of recentrange expansion patterns for M. leidyi. Invasion of regionsoutside its historical distributions have resulted in dramaticplanktonic community alterations in regions such as theBlack Sea (Shiganova et al. 2003) and Sea of Azov(Studenikina et al. 1991). Although perhaps less acclaimedthan these spatial range expansions, records of temporalrange expansion within its endemic range can also causeimportant changes in planktonic community dynamics(Sullivan et al. unpubl. data). For example, withinNarragansett Bay, peak occurrence of M. leidyi has shiftedapproximately 2 months earlier than the historic mean(Sullivan et al. 2001). However, the historically dominantsummer copepod, Acartia tonsa, has not experienceda similar phenological shift, with the result that theseasonal timing of predator (M. leidyi) and prey (A. tonsa)

overlap differently than during the past. One result of thischange is that A. tonsa has been almost eliminated from theplankton during recent summers in Narragansett Bay asa result of predation pressure from M. leidyi (Sullivan et al.unpubl. data). The long-term trophic consequences of nearremoval of copepods from Narragansett Bay duringsummer months, historically a period of high copepodabundance, are not yet clear. However, there is evidence ofreduction in numbers of some species of larval fish in recentyears (Keller et al. 1999) and increases in summer values ofchlorophyll a (Chl a) (Sullivan et al. unpubl. data).

Despite the potentially important consequences ofphenological shifts by M. leidyi, the mechanisms underlyingM. leidyi seasonality are not well documented. Metabolismand growth of M. leidyi are clearly influenced bytemperature (Kremer 1977), and climatic change has beensuggested (Sullivan et al. 2001) to underlie recent altera-tions in M. leidyi seasonality. The relationship is supportedby a positive correlation between periods of seasonaladvance in M. leidyi abundance and average sea surfacetemperature increases. However, the overall change inaverage annual temperature of 2uC over the last 50 yr inNarragansett Bay (Hawk 1998) appears relatively small toresult in such dramatic seasonality alterations. Likewise, itremains unclear why this level of warming has substantiallyaltered M. leidyi’s seasonality but not that of other co-occurring species.

We designed this program in order to describe seasonalpatterns in abundance and to clarify the mechanismsenabling temporal range expansion by M. leidyi. Previousresearch indicated that a general inshore–offshore gradientcharacterized the summer increase in M. leidyi abundanceand that seasonal population growth occurred first atinterior regions of Narragansett Bay (Kremer and Nixon1976). Our choice of sample locations reflected this

AcknowledgmentsWe thank A. Allen, C. Blackwelder, H. Chang, P. Ritacco, and

P. Schilling for field assistance during this research. P. Nortonallowed use of Norton’s Marina dock for sampling in GreenwichCove. J. Frietag provided a meter readout; URI’s GraduateSchool of Oceanography Marine Technical Service providedNiskin bottles. Tom Puckett operated the Capn’ Bert weeklythrough all conditions for the entire duration of sampling. We aregrateful to L. Mullineaux and two anonymous reviewers for theircomments and suggestions. Financial support for this researchwas provided by the National Science Foundation (OCE 9103309to J.H.C., OCE 0115177 to B.K.S., D.J.G.).

1 Corresponding author ([email protected]).

Limnol. Oceanogr., 51(4), 2006, 1819–1831

E 2006, by the American Society of Limnology and Oceanography, Inc.

1819

gradient and the parameters we measured were intended toclarify the basis for interstation differences in populationdynamics of M. leidyi.

Methods

Sample locations and frequency—Our sample locations(Fig. 1) represented a gradient spanning conditions fromthe mouth of Narragansett Bay to a sheltered embaymentwith restricted exchange to the main body of the bay. TheDutch Island site was near the mouth of Narragansett Bayand the Fox Island site further within the bay, but stillwithin a central water volume of Narragansett Bay (Pilson1985). Greenwich Cove is a highly sheltered embaymentwith extensive marina and recreational boat mooringactivity. Our goal was to sample along an inshore tomidbay gradient at several stations within a sufficientlyshort time duration to allow reasonable comparison amongstations. We chose a 3–4-h time duration for totalsampling. The time intervals between sampling events wereintended to be short enough to capture what preliminaryevidence indicated were events occurring on a timescale of

several weeks. Consequently, we sampled all three sites ona weekly basis for 2 yr (November 2001–October 2003).Inclement weather caused incomplete sampling once duringthe 2001–2002 season and four times during the 2002–2003season. Additionally, visual sampling for presence orabsence of M. leidyi was performed at six additional sitesduring winter of the 2001–2002 season and ice-free periodsof the 2002–2003 winter period.

Sample variables—A range of variables (Table 1) wasmeasured on each sample date at each site. Physicalvariables (temperature and salinity at 1-m depth intervals)were measured with a YSI Model 600SLM multiparametersonde. Water column stability was calculated by the indexE (Knauss 1997):

E ~a Ts { Tbð Þ

Dz

b Ss { Sbð ÞD

where a and b are constants (1.5 and 27.6, respectively); Ts

and Tb are temperatures at surface and bottom, respec-tively; Ss and Sb are surface and bottom salinity; and D isthe depth of the sample location.

Samples for Chl a were collected from a 2-liter Niskinbottle and/or a surface bucket. Typically, three depths weresampled when the water column was well mixed. Addi-tional depths were added when the water column wasstratified. Chl a samples were collected onto GF/F filters,extracted in 90% spectranalyzed acetone, and analyzed byfluorometry (Knap et al. 1996). Mesozooplankton werecollected by vertical tows of a 25-cm-diameter, 64 mm meshnet equipped with a flow meter. Vertical tows sampled theentire water column with the volume filtered varyingbetween 0.4–1.0 m3, depending on station depth. Thesamples were preserved in 5% formalin buffered withsodium borate. Subsamples containing at least 200individuals were counted under a dissecting microscope at350 magnification.

M. leidyi were collected by two oblique tows with a 0.5-m-diameter net (1-mm mesh) equipped with a flow meter.Tow duration ranged 3–10 min and was adjusted to collectsufficient numbers of ctenophores for appropriate statisti-cal analyses. These oblique tows sampled the entire watercolumn and volume sampled varied from 0.9 m3 to

Fig. 1. Locations of weekly sample stations and presence/absence visual surveys in Narragansett Bay, Rhode Island. M.leidyi were found to be present throughout the winter of 2001–2002 at all the visual survey stations.

Table 1. Summary of sample types and methods used duringthe survey.

Sample variable Method

Temperature YSI multiparameter sondeSalinity YSI multiparameter sondeChl a Niskin collection, fluorometryMesozooplankton composition

and concentration64-mm net collection, formalin

preservation, visualenumeration

M. leidyi abundance (,1.0-,.1.0-cm size fractions)

64- and 1,000-mm net collection

M. leidyi egg production Direct visual enumeration ofindividuals maintained foreither 24 or 48 h

1820 Costello et al.

79.0 m3, depending on station depth and abundance ofctenophores (when M. leidyi was very abundant, thevolume sampled was kept low to prevent net clogging,but when abundances were low in winter, the tow durationswere longer). The shallow depth and fixed sample platformat Greenwich Cove made such tows impractical at thatstation, so vertical tows were collected from the bottom tothe top of the water column.

The contents of the tow were counted and measuredimmediately (when possible) or returned to the laboratoryin a covered bucket for live measurements. M. leidyi eggproduction was measured on individuals collected by handand between 2 and 8 cm total length. A minimum of 5 butusually 15–35 individual animals were collected per station,returned to the laboratory in coolers, isolated in individualdishes in 300 mL of filtered seawater, and incubated for24 h at the temperatures of their capture locations. Attemperatures below 10uC, ctenophores were incubated for48 h, and the total egg production was divided by 2 to

obtain a daily rate. M. leidyi do not cannibalize their eggs(Kremer 1975), and container size during these shortincubations did not affect egg production rate (B. K.Sullivan unpubl. data).

Statistical comparisons between stations and years madeuse of the Statistica (Statsoft) software package. Repeated-measures analysis of variance (RM ANOVA) comparisonswere used for variables that were measured repeatedly ateach station on each sample date (e.g., Mnemiopsispopulation concentrations, temperature, zooplankton con-centrations). Standard ANOVA was used for comparisonsof variables that were not repeatedly measured at eachstation on each sample date (e.g., date of peak Mnemiopsisappearance, maximum or minimum yearly temperature).

Results

Physical characteristics of the sample sites—Seasonalvariations in temperature and salinity were similar in

Fig. 2. Physical characteristics, (A) temperature, (B) salinity, and (C) water column stabilityof sample sites during field study. Dashed line in (C) represents the threshold value of E (52.03 1024 m21) above which the water column is considered essentially stratified (Knauss 1997).

Mnemiopsis leidyi population patterns 1821

general pattern for all stations but more extreme at theinnermost station, Greenwich Cove, and least variable atthe outermost station near Dutch Island (Fig. 2). The FoxIsland station values typically lay between these twoextremes but were most similar to those of the DutchIsland station. Although Fox and Dutch stations werefrequently similar in many respects, the fact that they werecharacterized by different water masses was demonstratedby significantly different salinity and Chl a values for bothwinter and summer months from the two sites (ANOVA, p, 0.05). The 2 yr of sampling, designated by their summerperiods as 2002 and 2003, were historically warm and coldyears, respectively (NOAA 2004). Interannual variations inmaximum and minimum temperature were most pro-nounced at Greenwich Cove (Fig. 3). In contrast, themodifying effect of closer proximity to the Atlantic Oceanwas evident at the Dutch Island and, to a lesser extent, theFox Island stations.

The timing and patterns of spring warming variedsystematically across stations. Warming occurred earlierinshore than offshore during both sample years (Fig. 4;Table 2). We used the dates at which the 5uC, 10uC, 15uC,and 20uC thresholds were reached as an index of thetemporal variations of spring warming. The lowesttemperature threshold, 5uC, varied little between stationsin any year (Fig. 4; Table 2). Consequently, the averagedifference at which the 5uC threshold was surpassed wassmall (,5 d), between the innermost (Greenwich Cove) andoutermost stations (Dutch Island). However, this difference

increased at higher temperatures and, on average, Green-wich Cove warmed past the 15uC and 20uC thresholds 42 dand 24 d earlier, respectively, than Dutch Island station(Fig. 5A). However, temperature averages only partiallydescribe important differences between the thermal char-acteristics of the stations. Spring warming did not alwaysoccur at a uniform rate; instead, warming often occurred ina series of surges. The pulsed nature of spring warming wasmost evident in Greenwich Cove, and pulse amplitudedecreased toward the mouth of the bay. Warming-eventamplitudes at the Dutch Island station were highly dampedbetween 12–20uC. One striking example of between-stationdifferences in spring thermal pulses occurred during a surgecentered in mid-April 2002. The surge was evidentsimultaneously at all three stations (Fig. 4); however, therate of temperature increase at Greenwich Cove was twicethat at the Dutch Island station (Fig. 5C). As a consequenceprimarily of the higher rate of increase, temperatures inGreenwich Cove surged well into optimal reproductivetemperatures (pulse peak 5 18uC) compared with marginalreproduction temperatures (pulse peak 5 11.4uC) at theDutch Island site.

Fig. 3. (A) Maximum and (B) minimum sea surface tem-peratures at sample stations during the 2 yr of weekly sampling.

Fig. 4. Temperature records comparing spring warmingpatterns in 2002 and 2003 for each sample station.


Between-year variations in spring warming also contrib-uted substantially to the dates at which thermal thresholdswere passed. The largest differences between the warm yearof 2002 and the cold year of 2003 occurred in GreenwichCove at the 5uC threshold (Fig. 5B). However, the 15uCand 20uC thresholds were reached approximately 27 dearlier in the warm year of 2002 than the cold year of 2003.The between-year differences were less at the Dutch Islandand Fox Island stations (Table 2). Together, these dataindicate that seasonal warming patterns are relativelyconservative between years in the open bay, but thatembayments such as Greenwich Cove can experienceapproximately a month’s acceleration of spring warmingin the temperature ranges of 10–20uC during a warm year.

Salinity variations were most pronounced at GreenwichCove (Fig. 2B). Although these salinity variations werereflected across all the stations, their impact was lesspronounced at the Dutch Island station near the mouth ofNarragansett Bay.

Water column stratification, as indicated by the index E(Knauss 1997), was substantially higher at Greenwich Covethan at the open-bay stations (Fig. 2C). Frequent stratifi-cation at Greenwich Cove reflected both greater tempera-ture variations and, particularly during 2003, the stronginfluence of freshwater input as indicated by the corre-spondence between E and salinity values. In contrast, theDutch Island site was characterized by values of E thatwere below the threshold for stratification. These dataindicate that the Dutch Island station was generallycharacterized by a well-mixed water column, whereasGreenwich Cove was frequently stratified and the FoxIsland station was essentially intermediate between theother two stations.

Biological characteristics of the sample sites—Distinctdifferences were evident in the plankton communitiescharacterizing the sample stations. Phytoplankton standingstocks, measured as Chl a, were generally highest atGreenwich Cove, sometimes exceeding those of the DutchIsland station by an order of magnitude (Fig. 6A). The FoxIsland station chlorophyll standing stocks were of in-termediate levels but frequently resembled those of theDutch Island station.

Zooplankton assemblages were distinctly different be-tween Greenwich Cove and both open-bay stations.Copepods dominated the zooplankton numerically at bothFox Island and Dutch Island stations and copepodconcentrations were generally higher at these open-baystations than in Greenwich Cove (Fig. 6B). In contrast,rotifers and meroplanktonic larvae of polychaetes, mol-lusks, and barnacles typically dominated the zooplankton

Fig. 5. Patterns of spring warming during 2002 and 2003field seasons. (A) The increased rate of spring warming ina shoreward direction is demonstrated by the average difference,in days, between the dates at which the outermost site, the DutchIsland station, and the innermost site, the Greenwich Covestation, surpassed the same temperature thresholds. (B) Annualacceleration of spring warming, in days, between a warm year(2002) and a cold year (2003) at the innermost site, the GreenwichCove station. (C) Differences in the rate of temperature increaseduring a pulsed warming event (26 March–01 May 2002) that wasrecorded simultaneously at all three stations.

Table 2. Dates when temperature thresholds were reached orsurpassed during field sampling in Narragansett Bay.

Temperature(uC) Year

Station

DutchIsland Fox Island

GreenwichCove

5 2002 30 Jan 27 Feb 30 Jan2003 02 Apr 26 Mar 26 Mar

10 2002 17 Apr 17 Apr 10 Apr2003 07 May 30 Apr 30 Apr

15 2002 12 Jun 29 May 17 Apr2003 11 Jun 11 Jun 14 May

20 2002 01 Jul 01 Jul 29 May2003 09 Jul 02 Jul 25 Jun


of Greenwich Cove. Although the numerical abundance ofzooplankton was highest in Greenwich Cove for much ofthe period we sampled, total zooplankton concentrationswere often lower there during the summer months of Junethrough September, compared with the open-bay stations(Fig. 6C).

Mnemiopsis leidyi distribution patterns—M. leidyi ex-hibited strongly seasonal distribution patterns at all samplestations. Maximum M. leidyi concentrations occurredbetween the months of June and August during bothsample years at all stations (Fig. 7). Minimum populationlevels typically occurred during late winter or early spring(February–May) at all stations, and M. leidyi reachedundetectable levels during these times at the Fox and Dutch

Island stations. Although rapid population declines wereusually of this seasonal nature, local population declinescould occur in the midst of typically high abundanceperiods. For example, during 28 August–18 September2002, M. leidyi concentrations in Greenwich Cove droppedprecipitously during an intense algal bloom (Fig. 7C). Thisevent was not repeated in 2003.

Despite general seasonal similarities, there were impor-tant among-station differences in seasonal populationdemographics of M. leidyi in Narragansett Bay. The moststriking of these was the persistence of M. leidyi throughoutthe winters of 2002 and, for all but two sample dates, 2003at Greenwich Cove (Fig. 7C). This period included inter-vals with ice cover and temperatures below 1uC throughoutthe water column during which net tows through thin ice

Fig. 6. Biological characteristics, (A) Chl a concentration, (B) copepod abundance (includesnauplii, copepodites, and adults), and (C) total zooplankton abundance at sample sites duringfield study. Note the logarithmic scale in (C).


captured M. leidyi at this station. In contrast to thispersistence within Greenwich Cove, larval and adultconcentrations of M. leidyi declined to undetectable levelsat the open-bay stations of Fox and Dutch Islands duringlate winter and early spring (Fig. 7A,B). Adult (.1.0 cmtotal length) M. leidyi were irregularly present in Green-wich Cove during the late winter–spring of 2003, butreappeared more than a month earlier (14 May 2003) thanat the Fox and Dutch Island stations (25 June 2003). Larval(,1.0 cm total length) M. leidyi were less predictable intheir occurrence than adults and appeared regularly ata slightly earlier date (28 May) at the Dutch Island stationin 2003 than at the Fox Island station.

Populations of M. leidyi differed among stations inseveral other important aspects. In addition to appearingearlier in the spring (Fig. 8A), adult populations typicallypeaked later at Greenwich Cove than at the Fox or DutchIsland stations (Fig. 8B). An apparent gradient in the dateof peak abundance existed each year from the GreenwichCove to the Dutch Island station, but among-yearvariability obscured any significant between-station differ-ences (RM ANOVA, p . 0.05 for all comparisons). Adultpopulations of M. leidyi during peak summer months (01July–30 September) were significantly higher in GreenwichCove than at the Fox (RM ANOVA, p 5 0.04) or Dutch(RM ANOVA, p 5 0.01) Island stations. Average summer

Fig. 7. Concentrations of ctenophores (,1.0 cm, .1.0 cm, and combined) at each ofthe sample stations throughout the field study. Note the logarithmic scale used forctenophore concentrations.


concentrations of large M. leidyi were not significantlydifferent between the Fox and Dutch Island stations (RMANOVA, p 5 0.14). Average summer concentrations oflarge M. leidyi were higher in 2002 than 2003 at all stations,but the differences between years within any station werenot significant (RM ANOVA, all comparisons, p . 0.07).Patterns of average summer larval abundance were lesspredictable than those of adult M. leidyi because larvalpatterns differed between the two summers (Fig. 8C).Average summer concentrations were higher in 2002 than2003 at the Fox (ANOVA, p 5 0.002) and Dutch(ANOVA, p 5 0.016) Island stations, but not in GreenwichCove (ANOVA, p 5 0.578). High among-year variationobscured any effect of among station differences (Wilks,p 5 0.441) on average summer larval concentrations(Fig. 8C). Peak summer concentrations of large M. leidyi

were significantly higher in Greenwich Cove than at theFox (ANOVA, p 5 0.015) or Dutch (ANOVA, p 5 0.011)Island stations. Although there appeared to be a gradient inpeak adult concentrations extending from Greenwich Covemaxima to Dutch Island station minima in both sampleyears (Fig. 8D), among-year variability obscured anysignificant differences in peak summer adult abundancesbetween the Fox and Dutch Island stations (ANOVA, p 50.251). Peak summer abundances of larval M. leidyiparalleled average summer abundances. Consequently,peak summer concentrations of larval M. leidyi werehigher, but not significantly so, at Greenwich Covecompared with the Fox (ANOVA, p 5 0.074) and Dutch(ANOVA, p 5 0.080) Island stations.

Taken together, these results indicate that adult re-productive M. leidyi appeared earlier in the spring,

Fig. 8. Demographic traits of M. leidyi populations at sample sites during both sampleyears. (A) Dates of first appearance. (B) Peak abundance. (C) Average seasonal abundance.(D) Peak seasonal abundance during the summer (June–September).


persisted longer, and reached higher average and peakconcentrations in Greenwich Cove than at the Fox orDutch Island stations. Although inshore–offshore gradi-ents were evident in summer abundance patterns (date ofpeak, average, and peak concentrations), interannualvariation obscured differences between the two open-baystations. Consequently, these open-bay stations werestatistically indistinguishable for these variables. Larvalsummer abundance patterns were less clear with respect tostation and more strongly variable between years, render-ing conclusions about larval distribution patterns less clear-cut than those of adult M. leidyi.

Although Greenwich Cove was the only inshoreembayment that we sampled regularly, opportunisticsampling during the winter of 2002 at a variety of othersmall embayments along the northern periphery ofNarragansett Bay indicated that maintenance of over-wintering M. leidyi populations was not unique to Green-wich Cove. On the basis of presence/absence visual surveysof surface waters, a number of small embayments wereobserved to contain lobate M. leidyi throughout the wintermonths (Fig. 1). These six sites were usually visited twicemonthly during the winter of 2002, but heavy ice cover inthese shallow regions prevented collection of similar visualsurvey data during 2003.

Reproductive patterns of M. leidyi—Egg production byfield populations of M. leidyi was strongly temperaturedependent (Fig. 9). Very low rates of egg productionoccurred on some occasions at temperatures as low as6uC. However, substantial egg production characterized byrates of .10 eggs individual21 d21 did not occur below10uC, and rates were highest between 10uC and 25uC. The10uC temperature threshold was exceeded earliest in bothyears of sampling at Greenwich Cove (Fig. 2A), and eggproduction began earlier there each year than otherstations. Although temperatures .10uC were generallynecessary for high egg production, high temperature alonewas not sufficient to generate egg production because foodlimitation occurred frequently during warm summermonths (Sullivan et al. unpubl. data). As a result, evenduring warm periods, low egg production was common.

Migration between stations—Winter extinction periods atthe midbay stations were interrupted by ephemeral pulsesof adult, and in some cases larval, M. leidyi (Fig. 7). Theseunexpected occurrences were often followed by severalweeks when no M. leidyi were detected and temperatureswere below M. leidyi’s egg production threshold. Theabsence of adults at the open-bay stations during previousweeks and the low temperatures during the ephemeralpopulation pulses eliminated the explanation of rapidpopulation growth as the source of M. leidyi comprisingthese open-bay ephemeral pulses. Alternatively, advectivetransport from overwintering populations in embaymentssuch as Greenwich Cove could provide the ctenophorescomprising such ephemeral pulses. Demographic data areconsistent with this alternative explanation. The over-wintering population in Greenwich Cove possessed a similarsize frequency profile (x2, p 5 0.997) to that of the

ctenophores comprising an ephemeral pulse at the DutchIsland station the following week (24 April 2002 sample,Fig. 10).

Size frequency data indicate that the different stationswere experiencing different population phenomena duringthe same time interval. The Dutch Island station laggedbehind the overwintering Greenwich Cove population on17 April, and by 24 April Greenwich Cove had experienceda rapid warming event (Fig. 4A), egg production, andlarval recruitment (Fig. 10). Reproduction and recruitmentcontinued from that time into the summer at GreenwichCove but the Dutch Island station (and the Fox Islandstation as well, but not shown in Fig. 10) subsequentlyreturned to undetectable M. leidyi concentrations and didnot begin consistent population increase until 4 weeks laterin late May 2002. These data indicate that open-bayephemeral population pulses were characterized by sizefrequency distributions similar to those of overwinteringembayment populations such as Greenwich Cove, and thatspring population growth patterns at open-bay stationslagged several weeks behind that of the embaymentpopulation. The similarity in demographic traits betweenthe populations comprising open-bay pulses and theoverwintering population in Greenwich Cove suggests thatGreenwich Cove might be a source population for suchpulses; however, it is but one of a variety of overwinteringpopulations (Fig. 1) with potentially similar size frequencypatterns that occur in other sections of Narragansett Bay.

Discussion

Embayments as source population regions—GreenwichCove served as a winter refuge for M. leidyi (Fig. 7), andpreliminary evidence from other shallow embayments(Fig. 1) indicates that this phenomenon was common alongthe margins of Narragansett Bay. Even during a coldwinter (2003) with widespread ice cover, M. leidyi werefound in Greenwich Cove on all but two sample dates.Earlier spring warming enabled the Greenwich Cove

Fig. 9. Egg production of M. leidyi in relation to thetemperature at which they were collected in the field.


population to grow and reproduce weeks earlier than open-bay stations (Figs. 10, 11). The sudden arrival of fullygrown adults at the open-bay stations during winter andspring suggests that these embayment refugia serve assource populations from which advective transport pro-vides inocula for the open regions of the bay. Theseadvective transport events occurred irregularly throughoutthe winter of 2002, but successful establishment ofpersistent populations in the open bay occurred only afterthe latter regions warmed sufficiently to allow reproduc-tion. Before reaching these temperatures, pulses likely wereephemeral because the thermal physiology of M. leidyi

constrains reproductive potential and the ctenophores hadno mechanism for population replacement to counteradvective losses caused by high average flushing rates inNarragansett Bay (Pilson 1985). Once temperature limita-tion was relaxed by spring warming throughout the bay,the dramatic feeding (Reeve et al. 1978; Kremer 1979) andreproductive capacities (Kremer 1975; Sullivan unpubl.data) of M. leidyi allowed rapid colonization and popula-tion expansion throughout the bay.

It is important to note that the relative advantagesenjoyed by Greenwich Cove populations of M. leidyi werenot limited to winter and spring. Average and peak summerconcentrations were significantly higher in Greenwich Covethan the open-bay stations. Reproduction began earlier,reached higher average and peak levels, and lasted longer inGreenwich Cove than the open-bay stations. During the2 yr of this study, Greenwich Cove, and presumably otherembayments, served as refugia from which M. leidyipopulations could expand during favorable summerperiods and to which populations contracted duringunfavorable winter periods. In contrast, open-bay stationswere characterized by predictable seasonal extinctions(reductions to levels below detection) during each winter.

The different dynamics characterizing populations of M.leidyi existing in different regions of the bay correspond topatterns described by metapopulation theory. A metapop-ulation is a population of populations linked by dispersal(Hanski 1999). The source-sink metapopulation model(Pulliam 1988) describes source regions as those occupiedby populations with positive local recruitment which, viamigration, supplement sink regions characterized by long-term net negative growth and frequent local extinction. Theexpansion from source regions during favorable environ-mental periods may encompass multiple sink regions anda large proportion of the total metapopulation range canexist in sink habitats if the source regions are sufficientlyproductive to subsidize the larger sink regions. Greenwich

Fig. 10. Size frequency distributions of M. leidyi during anepisodic occurrence at Dutch Island (open-bay station) in contrastto Greenwich Cove (embayment station) during the same period.

Fig. 11. Correspondence of M. leidyi egg production with pulsed temperature events duringthe spring of years 2002 and 2003.


Cove and other embayments along the bay’s marginprovide persistent winter refugia and, via advective trans-port, inocula for summer growth in open-bay areas such asthe Fox and Dutch Island stations. Population growth canbe rapid in these open-bay areas under favorable summerconditions, but is subsequently followed by seasonalextinction when temperature-limited reproduction and highwinter flushing rates inevitably result in seasonal extinctionin the open bay.

The source-sink perspective is consistent with seasonaldistribution patterns described by previous studies inNarragansett Bay as well as in other regions of the worldpersistently occupied by M. leidyi (Table 3). Sourceregions, particularly in temperate regions with cold winters,are suggested by seasonal population expansion fromnearshore regions in areas as diverse as New England(Kremer and Nixon 1976), Argentina (Mianzan andSabatini 1985), and the Black Sea (Shiganova et al. 2001).Studies permitting delineation of M. leidyi source and sinkregions are limited in number because this distinctionrequires multiyear sampling regimes of sufficient spatialvariation to distinguish different types of habitat withina metapopulation region.

What variables distinguish source from sink habitats?—Hydrographic characteristics are probably the criticalvariables distinguishing source habitats within metapopu-lations of M. leidyi living in temperature regions charac-terized by cold (,10uC) winter sea temperatures. Docu-mentation of most parameters integral to populationdynamics, such as natality, mortality, immigration, andemigration, are difficult for a holoplanktonic species suchas M. leidyi existing in a dynamic hydrographic environ-ment such as Narragansett Bay. Instead, we delineatesource habitats by seasonal persistence—population sourcehabitats persist through annual seasonal cycles, while sink

regions experience local extinctions each winter. Refugiaallowing overwintering are crucial to M. leidyi because,unlike many other neritic plankton, the entire life cycle isplanktonic and does not include any overwintering cyst orbenthic stages. Flushing and advective transport areimportant factors in population persistence because thereare long winter periods (.90 d) when water temperaturesare below the physiological threshold for reproduction and,therefore, replacement of individuals lost through advec-tion is not possible. Flushing rates are strongly affected bywinds, tidal variations, and freshwater input; but averageestimates of residence times (duration of time that a parcelof water resides in a location) for Narragansett Bay areshort (28 d—Pilson 1985; 43 d—Abdelrhman 2005) com-pared with the winter nonreproductive interval of M. leidyi.However, not all regions of the bay are hydrographicallyequivalent and some areas experience much longer localresidence times than the baywide mean values (Abdelrh-man 2005). Source regions may simply be those regions,such as Greenwich Cove, characterized by comparativelylong local residence times that allow sufficient retention ofM. leidyi to survive winter nonreproductive months. Thischaracterization could include a variety of regions withcomparatively long residence times, whether in shallowembayments with limited exchange to the open bay, such asGreenwich Cove, or retention features such as gyres withinthe open bay.

We envision source-sink interactions affecting localmetapopulation dynamics and operating within tempera-ture and feeding constraints that determine global patternsof M. leidyi seasonality and abundance. Kremer (1994)described the relationship between temperature and foodavailability patterns with large-scale patterns of M. leidyiseasonality. These physiologically based patterns apply toM. leidyi in both source and sink regions within Narra-gansett Bay. For example, only when temperatures rise

Table 3. Annual patterns of Mnemiopsis leidyi distributions sharing metapopulation traits with the current study.

Region Seasonal variation pattern Reference

Narragansett Bay, USA Providence River regions characterized by longerseasonal presence and higher average abundancesthan the mouth of the bay bordering the AtlanticOcean. Spring growth spread from inshore to offshorestations.

Kremer and Nixon (1976)

Black Sea Spring population growth earliest at nearshorestations with subsequent seaward spread during2-yr sampling period.

Shiganova et al. (2001)

Aral Sea Annual reintroduction necessary from adjoiningBlack Sea due to yearly winter extinction in theAral Sea.


Sea of Marmosa Persistent year-round population provides a sourceregion for annual colonization of adjoining areasvia advective transport


Bahia Bay, Argentina Winter persistence of M. leidyi in core region of bayoccupied by a cluster of islands. Seasonal populationexpansion from this core region during summer monthsfollowed by contraction to core region during wintermonths over a 3-yr period.

Mianzan and Sabatini (1985)


above the 10uC threshold for egg production do popula-tions increase either at Greenwich Cove or the open-baystations. Likewise, reproduction declines and overallpopulation sizes decrease at all stations in midsummerwhen zooplankton availability diminishes (Sullivan unpubl.data). However, neither temperature nor food availabilityare likely to determine the role of Greenwich Cove andother embayments as source regions within the Narragan-sett Bay metapopulation of M. leidyi. Minimum wintertemperatures are less favorable for M. leidyi at GreenwichCove than the open-bay stations (Fig. 3B). Likewise, wintercopepod concentrations are frequently lower in GreenwichCove than the open-bay stations (Fig. 6B). Therefore,although temperature and food availability affect M. leidyithroughout Narragansett Bay, just as they do in otherregions (Kremer 1994), the relative roles of source and sinkhabitats within Narragansett Bay are most likely de-termined by hydrographic traits that determine retentiondurations. This is because retention durations most directlyaffect winter population persistence in a region and it ispopulation persistence that primarily distinguishes theGreenwich Cove source habitat from open-bay sinkhabitats.

Metapopulation interactions with climate change—Thesource-sink perspective permits a mechanistic understand-ing of climatic effects upon M. leidyi seasonality inNarragansett Bay. It does so by establishing a relationshipbetween the local effects of warming and the populationstructure of M. leidyi. The global process of climatewarming is expressed locally in Narragansett Bay throughspring warming surges whose amplitudes are magnifiedwithin shallow embayments (Figs. 4, 5). This shorewardthermal amplification is maximized within the sourceregions containing overwintering populations of M. leidyi.Shoreward thermal amplification results in temperaturespikes within source habitats that exceed temperaturethresholds for reproduction and M. leidyi responds tothese pulsed warming events with pulsed reproductiveevents (Fig. 11). Once these spring reproductive events areinitiated, reproduction continues into the summer andgenerates high population concentrations in source regionsmore than a month prior to sink regions (Fig. 7). Advectiveevents likely transport ctenophores from source to sinkregions (Fig. 10). Rapid population expansion throughoutthe bay can then occur when sink region temperaturesexceed the thermal reproductive limits of M. leidyi. Thisearly expansion typically coincides with high zooplanktonavailability (Fig. 6) that provides the nutritional sourcefueling M. leidyi’s high reproductive capabilities (Kremer1975).

The synergistic interaction between source-sink popula-tion dynamics of M. leidyi and shoreward thermalamplification is rooted in local-scale interactions that arenot described well by global temperature averaging. Ouroriginal research approach sought to determine themechanism whereby a 2uC increase in average annualtemperature could produce a phenological shift by M.leidyi of approximately 2 months. Our results suggest thatboth the location and time duration of the 2uC average

increase may underemphasize the importance of climatechange on M. leidyi in Narragansett Bay. The 2uC increaserepresents an average annual temperature increase atNewport, near the mouth of Narragansett Bay (Sullivanet al. 2001). However, shallow embayments are affectedmore dramatically by variations in air temperature thanopen-bay stations near the bay mouth (Fig. 5C). This isimportant for M. leidyi seasonality because it is thetemperatures in source embayments, such as GreenwichCove, not sink regions of the open bay near the bay mouth,such as the Newport region, that determine the onset ofseasonal reproduction for the Narragansett Bay metapop-ulation of M. leidyi. A second factor influencing the utilityof the 2uC Newport increase is the time duration of theaverage. Spring (March–June) is the relevant time periodfor examining between-year variation in the onset of M.leidyi seasonal growth (Sullivan et al. 2001) and averagetemperatures for these spring months are the most usefulindicators of the difference in M. leidyi seasonalityobserved in Greenwich Cove between 2002 and 2003. Incontrast, annual averages for 2002 and 2003 from the samestation (Greenwich Cove) include many irrelevant datescausing important between-year patterns to be masked.Given these qualifications regarding location and durationof temperature averaging, it is not surprising that a 2uCannual increase in average temperature at Newport couldresult in major phenological shifts by M. leidyi. Such anaverage annual temperature change near the bay mouthcould result in dramatic alterations in spring temperatureregimes that would be highly amplified in shallow embay-ments (Fig. 5) serving as M. leidyi source habitats.

The effect of climatic changes on M. leidyi’s seasonalityis linked to the ctenophore’s particular population dynam-ics. However, the same environmental changes might affectanother species very differently if it possessed differentpopulation dynamics. For example, species with populationcenters located in open-bay regions would not be asstrongly affected by shoreward thermal amplification andtherefore might experience little phenological variationduring the same period for which M. leidyi’s phenologychanged dramatically. The net result of different species-specific responses to environmental variation is expressedat the community level as trophic mismatching (Edwardsand Richardson 2004) and can result in importantcommunity-level alterations (Sullivan et al. unpubl. data).Understanding, and ultimately predicting, community-levelalterations will require identification of the critical interac-tions governing how individual species respond to envi-ronmental change.

References

ABDELRHMAN, M. A. 2005. Simplified modeling of flushing andresidence times in 42 embayments in New England, USA,with special attention to Greenwich Bay, Rhode Island. Est.Coastal Shelf Sci. 62: 339–351.

EDWARDS, M., AND A. J. RICHARDSON. 2004. Impact of climatechange on marine phenology and trophic mismatch. Nature430: 881–885.

HANSKI, I. 1999. Metapopulation ecology. Oxford Univ.Press.


HAWK, J. D. 1998. The role of the North Atlantic Oscillation inwinter climate variability as it relates to the winter–springbloom in Narragansett Bay. M.S. thesis, Univ. of RhodeIsland.

KELLER, A. A., G. KLEIN-MACPHEE, AND J. S. ONGE BURNS. 1999.Abundance and distribution of ichthyoplankton in Narra-gansett Bay, Rhode Island, 1989–1990. Estuaries 22: 149–163.

KNAP, A., A. MICHAELS, A. CLOSE, H. DUCKLOW, AND A. DICKSON,[eds.]. 1996. Protocols for the Joint Global Ocean Flux Study(JGOFS) Core Measurements. JGOFS Report No. 19. Re-print of the IOC Manuals and Guides No. 29, UNESCO1994.

KNAUSS, J. A. 1997. Introduction to physical oceanography, 2nded. Prentice-Hall.

KREMER, P. 1975. The ecology of the ctenophore Mnemiopsisleidyi in Narragansett Bay. Ph.D. thesis, Univ. of RhodeIsland.

———. 1977. Respiration and excretion by the ctenophoreMnemiopsis leidyi. Mar. Biol. 44: 43–50.

———. 1979. Predation by the ctenophore Mnemiopsis leidyi inNarragansett Bay, Rhode Island. Estuaries 2: 97–105.

———. 1994. Patterns of abundance for Mnemiopsis in the U.S.coastal waters: A comparative overview. ICES J. Mar. Sci. 51:347–354.

———, AND S. NIXON. 1976. Distribution and abundance of thectenophore, Mnemiopsis leidyi in Narragansett Bay. Estuar.Coastal Mar. Sci. 4: 627–639.

MIANZAN, H. W., AND M. B. SABATINI. 1985. Estudio preliminarsobre distribucion y abundancia de Mnemiopsis maccradyi enel estuario de Bahia Blanca, Argentina (Ctenophora).Spheniscus 1: 53–68.

NOAA. 2004. Northeast region climate summary [Internet].[Accessed 10 March 2006.] Available from http://www.ncdc.noaa.gov/oa/climate/research/cag3/nt.html

PILSON, M. E. Q. 1985. On the residence time of water inNarragansett Bay. Estuaries 8: 2–14.

REEVE, M. R., M. A. WALTER, AND T. IKEDA. 1978. Laboratorystudies of ingestion and food utilization in lobate andtentaculate ctenophores. Limnol. Oceanogr. 23: 740–751.

SHIGANOVA, T. A., E. I. MUSAEVA, Yu. V. BULGAKOVA, Z. A.MIRZOYAN, AND M. L. MARTYNYUK. 2003. Invaders cteno-phores Mnemiopsis leidyi (A. Agassiz) and Beroe ovata Mayer1912, and their influence on the pelagic ecosystem of thenortheastern Black Sea. Biol. Bull. 2: 180–190.

———, AND oTHERS. 2001. Population development of the invaderctenophore Mnemiopsis leidyi, in the Black Sea and in otherseas of the Mediterranean basin. Mar. Biol. 139: 431–445.

STUDENIKINA, Y. E. I., S. P. VOLOVIK, I. A. MIRZOYAN, AND G. I.LUTS. 1991. The ctenophore Mnemiopsis leidyi in the Sea ofAzov. Oceanology 31: 722–725.

SULLIVAN, B. K., D. VAN KEUREN, AND M. CLANCY. 2001. Timingand size of blooms of the ctenophore Mnemiopsis leidyi inrelation to temperature in Narragansett Bay, RI. Hydro-biologia 451: 113–120.

WAGGETT, R., AND J. H. COSTELLO. 1999. Different mechanismsused by the lobate ctenophore, Mnemiopsis leidyi, to capturenauplii and adult life stages of the copepod Acartia tonsa. J.Plankton Res. 21: 2037–2052.

Received: 13 February 2005Accepted: 14 November 2005

Amended: 1 March 2006


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