Numerical Increases and Distributional Shifts of Chrysaora Quinquecirrha (Desor) and Aurelia Aurita (Linne)´ (Cnidaria: Scyphozoa) in the Northern Gulf of Mexico

Home , Carybdea, Chrysaora quinquecirrha

Numerical increases and distributional shifts of Chrysaora quinquecirrha (Desor) and Aurelia aurita (Linne)´ (Cnidaria: Scyphozoa) in the northern Gulf of Mexico

W. M. Graham Dauphin Island Sea Lab and Department of Marine Science, University of South Alabama, 101 Bienville Blvd, Dauphin Island, AL, 36528, U.S.A. E-mail: [email protected]

Key words: jellyﬁsh, medusae, Mississippi River, SEAMAP, eutrophication, hypoxia

Abstract Fisheries resource trawl survey data from the National Marine Fisheries Service from a 11–13-year period to 1997 were examined to quantify numerical and distributional changes of two species of northern Gulf of Mexico scyphomedusae: the Atlantic sea nettle, Chrysaora quinquecirrha (Desor), and the moon jelly, Aurelia aurita (Linné). Trawl surveys were grouped into 10 statistical regions from Mobile Bay, Alabama to the southern extent of Texas, and extended seaward to the shelf break. Records of summertime C. quinquecirrha medusa populations show both an overall numerical increase and a distributional expansion away from shore in the down-stream productivity field of two major river system outflows: Mobile Bay and the Mississippi-Atchafalaya Rivers. In addition, there is a significant overlap between summer C. quinquecirrha and lower water column hypoxia on the Louisiana shelf. In trawl surveys from the fall, A. aurita medusae showed significant trends of numerical increase in over half of the regions analyzed. For both species, there were statistical regions of no significant change, but there were no regions that showed significant decrease in number or distribution. The relationships between natural and human-induced (e.g. coastal eutrophication, fishing activity and hard substrate supplementation) ecosystem modifications are very complex in the Gulf of Mexico, and the potential impact of increased jellyfish populations in one of North America’s most valuable fishing grounds is a most critical issue. Several hypotheses are developed and discussed to guide future research efforts in the Gulf of Mexico.

Introduction Increased jellyfish production in marine ecosystems is perhaps a symptom of larger ecosystem de- The role of jellyfish in long-term ecosystem change gradation due to coastal eutrophication and over- is receiving increased attention. A number of mar- fishing (Caddy, 1993; Mills, 1995). During ‘bloom’ ine ecosystems, identified by Mills (2001) have either events, jellyfish are capable of exerting considerable documented or suspected cases of long-term eco- control over the flow of energy and nutrients through logical variations that involve jellyfish populations. the ecosystem due to extremely high consumption However, systematically collected, long-term data- rates (Purcell, 1989, 1992, 1997). As such, coastal sets involving jellyfish numbers or biomass are rare. seas with a high degree of susceptibility to eutrophic- Among the notable cases where ecological change is ation and with high fisheries yields should be closely best documented with respect to jellyfish are the Black watched for similar ecological change. Yet, again, the and Azov Seas (Kideys, 1994; Kovalev & Piontkovski, availability of existing long-term data-sets involving 1998; Shiganova, 1998; Purcell et al., 2001), the Ber- jellyfish numbers is rare. ing Sea (Brodeur et al., 1999) and the Mediterranean The northern Gulf of Mexico continental shelf is Sea (Goy et al., 1989). among the most productive and highly fished regions 98 of North America. Pulsed delivery of nutrients to the The goal of the present study is to analyze more Gulf of Mexico through the Mississippi River Delta than 10 years of data from large-scale trawling efforts and numerous other river-dominated estuaries of the in the northern Gulf of Mexico. These fishery resource northern Gulf account for a cumulative regional estu- survey data will be used to assess long-term vari- arine surface area of 30 000 km2. The drainage area ations in two important jellyfish species: the Atlantic emptying into the Gulf of Mexico is over 4 mil- sea nettle, Chrysaora quinquecirrha (Desor), and the lion km2 or approximately 55% of the conterminous moon jellyfish, Aurelia aurita (Linné). Similar ana- United States with the Mississippi River and Mo- lyses of fisheries trawl data have been used previously bile Bay estuary discharging the 1st and 4th largest to identify long-term changes of jellyfish populations volumes, respectively. To complicate ecological vari- in the Bering Sea (Brodeur et al., 1999). ations, the Gulf of Mexico yields about 1/3 of the total United States fishery production and supports the largest fishery by volume in North America in the Methods planktivorous Gulf Menhaden, Brevoortia patronus. Fluvial discharge of nutrients directly onto the SEAMAP trawl data-set shelf is responsible for the high production rates (Lohrenz et al., 1997). Rivers and estuaries of the The data presented in this analysis are from the United northern Gulf of Mexico, from the Florida panhandle States National Marine Fisheries Service (NMFS) to southern Texas (Fig. 1), discharge the greatest Southeast Area Monitoring and Assessment Program volume of water during winter and spring months. (SEAMAP) managed through the Southeast Fisheries Low estuarine residence times due to high freshwater Science Center in St. Petersburg, Florida. The spe- discharge and typically shallow estuarine geomorpho- cific subset of data used for this study were collected logy rapidly displace nutrients and production out onto as part of the twice-yearly shrimp/groundfish surveys the shelf (Pennock et al., 1999). The greatest sea- from 1985 to 1997 in the northern Gulf of Mexico sonal primary production rates in the northern Gulf of between Mobile Bay, Alabama and the southern bor- Mexico are associated with the Mississippi-Atchafalya der of Texas. Though SEAMAP shrimp/groundfish River system and Mobile Bay estuary outflows; pro- surveys were initiated in 1982, I have omitted 1982– ductivity rates are depressed accordingly with the 1984 entirely from analysis because of inconsistent lower-discharge estuaries of Texas (reviewed in Pen- coverage. nock et al., 1999). Zooplankton grazing and secondary The SEAMAP shrimp/groundfish survey protocol production are intense at the coastal transition zone is detailed in Stuntz et al. (1985). In summary, surveys (Dagg & Whitledge, 1991; Dagg, 1995; Ortner & over the entire sampling area were divided into 11 stat- Dagg, 1995) and trophic transfer of this energy to istical regions. Only NMFS designated regions 11 and fish is highly coupled to estuarine delivery in the Gulf 13 through 21 were used; regions 1–10 east of this area (Deegan et al., 1986). The alternate pathway of en- did not have shrimp/groundfish survey data, and re- ergy to gelatinous zooplankton predators has thus far gion 12 was only occasionally surveyed. Surveys were received little, if any, attention. conducted twice-annually: once in the summer (May– The historical lack of interest in the ecological role July) and once in the fall (October–November). Trawl of jellyfish is surprising. The Gulf of Mexico supports sites (typically 30–50 trawls per statistical region per among the greatest diversity of pelagic cnidarians in survey) were randomly located within each region in the world. Over 115 epipelagic species were listed 5 depth strata. The location of stations within depth by Phillips (1971) including 16 species of Scypho- strata caused sampling frequency to be higher near the zoa and Cubozoa. Given that Phillips’ (1971) synopsis coast but consistent between regions and years. An is nearly 30 years old and lacks deep-water inform- example of station density and arrangement (for fall ation, certainly this number severely under-estimates 1991) is given in Figure 1. A preliminary analysis of the real diversity. Given such diversity and potential variance was performed as a check on the randomness importance of jellyfish in this very productive sys- of distribution within and between statistical regions tem, long-term data on jellyfish variations are crucial and depth strata in order to avoid errors in the inter- for realizing current or future ecological changes as pretation of the data. Because of this, I eliminated identified by Caddy (1993) and Mills (1995). statistical region 12 entirely from the study, and the years 1985–1986 from analysis of the summer trawls. 99

Figure 1. Map of study region in the northern Gulf of Mexico. Boxes indicate 10 statistical regions of the SEAMAP sampling program. Points within the boxes are an example of station distribution for a single trawl series in the Fall of 1991 (446 stations). The 20 m and 40 m isobaths are indicated with heavy lines.

Table 1. Summary of SEAMAP trawls conducted in the northern sizes large enough to be captured in the trawl net- Gulf of Mexico from 1985 to 1997. Chrysaora quinquecirrha medusae were analyzed only from summer trawls and Aurelia aurita ting, and they are hardy enough to be retained without medusae were analyzed from fall trawls so much damage that they are unrecognizable or un- countable. Chrysaora quinquecirrha medusae occur Year No. Trawls Collected during summer months in the Gulf of Mexico with Summer Fall peak abundance usually in June–July (Burke, 1975, 1985 ··· 404 1976). Some reporting of ‘Dactylometra quinquecir- 1986 ··· 236 rha’ from Texas regions has been combined with the 1987 615 365 C. quinquecirrha since these are widely considered 1988 500 701 to be the same species. Aurelia aurita medusae occur 1989 359 631 during the fall months with peak abundance usually in 1990 432 451 October–November (Burke, 1975, 1976). Therefore, 1991 433 446 analysis of C. quinquecirrha is limited to the summer 1992 420 364 surveys (1987–1997) and A. aurita is limited to fall 1993 454 402 surveys (1985–1997). As seen in the trawl summary of 1994 483 380 Table 1, over 10 000 individual trawls were included in 1995 363 337 the present analysis. 1996 388 438 Numerical trawl data are reported here as a stand- 1997 365 377 ardized catch. Other studies have used indexed trawl Total 4812 5532 data in this fashion (Brodeur et al., 1999), and a standardized trawl allows for sufficient comparison between years and between regions even if some differences in gear or vessels existed. Most collections were made I limited the present study to the two species of with a standard 12 m wide shrimp trawl for a max- scyphomedusae that are most abundant and widely imum 60 min tow. In some nearshore cases, a 5 m distributed throughout the northern Gulf of Mexico. In wide trawl was used; these data have been standard- addition to their prevalence, both species also reach 100 ized to a 12 m swath. All data were standardized those average catches tended to increase or decrease to a 60 min trawl. The trawl and cod-end mesh was with sample year. nominally 2.5 cm (fully stretched). Since, the typical Variations of jellyfish distribution within a statist- size of Chrysaora quinquecirrha medusae during mid- ical region were determined as changes in frequency summer is about 10 cm and Aurelia aurita medusae in all trawls within a region that recorded either is 35–40 cm (Phillips, 1971), it is assumed that at Chrysaora quinquecirrha or Aurelia aurita. Change in least individuals larger than 5 cm of both species were distribution in the cross-shelf direction is an import- retained in the trawl. ant consideration for determining whether numerical Numerical recording of all by-catch by taxon has changes of jellyfish reflect increased local abundance been consistent during the SEAMAP surveys, how- or whether there has been a distributional expansion ever, the trawls were conducted for the purpose of across the shelf. Expansion of the population’s dis- collecting shrimp and groundfish on the sea floor. tribution from shore was determined by frequency of Therefore, collections of jellyfish and other water species occurrence in trawls from stations in less than column fauna should be viewed with some degree 20 m total water depth or greater than 20 m water of caution, since they were not target species. The depth. expectation here is that the large number of trawls collected over a long period of time will allow a ro- bust view of changes in numbers and distributions of Results jellyfish. Also, the jellyfish data reflect an integrated sample of the entire water column. As such, they must Variations in jellyfish numbers be interpreted as an integrated or areal concentration of jellyfish rather than as a volumetric concentration. Time-series of jellyfish catches in summer (Chrysaora Some biomass and length data are available for jelly- quinquecirrha)andfall(Aurelia aurita) are plotted as fish collected in trawls, but these are not consistent regional averages each year (Figs 2 and 3). Qualitat- over the same time frame, and I chose to omit them ively, and independent of longer trends, the magnitude from this analysis. of year-to-year variations in regional A. aurita density Dissolved oxygen records from the SEAMAP was greater than that of C. quinquecirrha variations. database also were used in the present analysis. Water Log-transformed data in Figures 2 and 3 are used to samples from the lower water column were collected resolve better the long-term trends. Variations in re- by NMFS scientists using Niskin-type bottle samplers. gional A. aurita densities between consecutive years Dissolved oxygen was measured either by polaro- frequently vary by as much as an order of magnitude; graphic oxygen probe or by Winkler titration. Oxygen similar magnitude variations in C. quinquecirrha were probes were calibrated by the air saturation technique less frequent. It is apparent that differences in number prior to each cruise. Specific sampling technique de- and pattern are not consistent across statistical regions pended on participating institutional resources, how- within or between species. It is important, therefore, to ever, measurements were primarily made with YSI separate statistically those regions that exhibit consist- Oxygen Probes. ent long-term changes from those regions that simply have large year-to-year variations. Only regions 15 and 16 experienced statistically Analytical considerations significant long-term (defined as the entire period of study) numerical increase of Chrysaora quinquecirrha The standardized catch data used to derive means and (rank order test, p <0.05). Proximity of regions 15 and standard deviations presented in Figures 2 and 3 were 16 suggests that this increase may have been over a not conducive to traditional parametric analyses des- larger, contiguous area of the Louisiana shelf of the pite attempts to normalize the data through various northern Gulf of Mexico. In regions 15 and 16, C. transformations. In order to test whether variations quinquecirrha medusae were absent prior to 1992, but in jellyfish populations increased or decreased with between 1992 and 1997, they increased numerically time, an alternative non-parametric Spearman rank- by as much as 2 orders of magnitude. order analysis was employed. This was accomplished Despite lack of significance in the long-term trend by using the regionally averaged standard catch data in other regions, a particularly interesting numerical presented in Figures 2 and 3 and then testing whether jump in Chrysaora quinquecirrha also occurred at 101

Figure 2. Standardized catch of Chrysaora quinquecirrha from summer SEAMAP trawl samples, 1987–1997, in each statistical region identified in Figure 1. Solid lines represent the mean catch; the dashed line represents one standard deviation above the mean. An asterisk ∗ beside the region number ( ) indicates significant increase with time at p<0.05. Standardized catch reflects a 60 minute trawl using a 12 m wide trawl. 102

Figure 3. Standardized catch of Aurelia aurita from fall SEAMAP trawl samples, 1987–1997, in each statistical region identified in Figure 1. AllelseasinFigure2. 103 regions 11, 13 and 14 in the northern Gulf (Fig. 2). Re- >20 m trawl stations is assumed to represent offshore gion 11 at the eastern extent of the study area showed a expansion of the population. dramatic increase by two orders of magnitude in 1992, Overall, Chrysaora quinquecirrha medusae exhib- yet only a statistically marginal long-term increase in ited a trend toward increased distribution offshore in 4 this species with time (rank order analysis, p = 0.055). of the 10 statistical regions, which is in contrast to the However, in region 11, this transition marked a period numerical increases in only 2 regions. Between 1987 when C. quinquecirrha densities remained consist- and 1992 in regions 11–16 (Alabama–Louisiana), C. ently higher than pre-1992 numbers (Fig. 2). Region quinquecirrha occurred only rarely and was never re- 13, near the outflow of the Mississippi river, recorded corded at stations seaward of the 20 m isobath (Fig. C. quinquecirrha only in 1992. This species was not 4). In 1992, however, frequency of C. quinquecirrha recorded in Region 14 from 1987 to 1991, however, occurrence in trawl collections increased markedly at their appearance in 1992 in region 14 marked a 5 year both inshore and offshore stations on the Alabama- period of presence. Significant trends of C. quinque- Louisiana shelf. For C. quinquecirrha, distributional cirrha densities did not occur to the west of region 16 expansion with time was significant throughout re- on the Texas shelf. With the exception of region 21 gions 11, 15 and 16 (Table 2). By 1997, C. quinque- at the southwestern extent of the study area, C. quin- cirrha were recovered from 20 to 25% of all trawl quecirrha was usually present in varying abundance stations in regions 11, 15 and 16; 40–75% of these in all years (Fig. 2). The apparent cycling of medu- stations were seaward of the 20 m isobath. Interest- sae of this species in regions 19 and 20 (and possibly ingly, although few C. quinquecirrha were recovered 21) is note-worthy and seems consistent among these in region 13 during 1992, they occurred in more than adjacent regions, but independent of variations in any 30% of all trawl stations in that region (Fig. 4). To the other region. west of region 16 (i.e. the Texas shelf), the only off- Significant trends of numerical Aurelia aurita inshore shift of C. quinquecirrha was in region 17, but crease occurred in 6 of the 10 statistical regions this did not result in an overall increase in frequency (Fig. 3). Regions 13, 14 and 16 on the Louisiana of occurrence (Table 2). Chrysaora quinquecirrha was shelf showed a 5–10-fold increase A. aurita densities widely distributed among stations within all statistical between the mid 1980s and the mid 1990s; in fact, the regions on the Texas shelf during all years with the species was virtually absent over much of the study exception of region 21. area in the 1980s compared with densities of the mid- Significant shifts toward offshore distribution of 1990s. Toward the Texas shelf, regions 17, 18 and 20 Aurelia aurita medusae occurred in only 3 of the 10 each showed nearly a two order of magnitude increase statistical regions, which contrasts with numerical in- from 1985 to 1986 numbers by 1997. Particularly increases in 6 of the regions. Since the study began in teresting features across most of the study area were 1985, A. aurita has been widely distributed across the consistent depressions in A. aurita densities in 1988 study area (Fig. 5). Significant trends of increased and 1994 across the study area. catch frequency of A. aurita occurred from the mouth of the Mississippi river to the northeastern Texas coast (regions 13, 15–18). In these five regions, the mag- Distribution shifts nitude of increased frequency of A. aurita occurrence ranged from 2-fold to more than 10-fold between 1985 Variations in the distribution of summer Chrysaora and 1997. The majority of this increase in overall quinquecirrha and fall Aurelia aurita medusae are frequency with time can be explained by increased presented in Figures 4 and 5. The data in these figures frequency of occurrence at stations inshore of the 20 are summarized into three trawl-depth categories (0– m isobath (i.e. no offshore expansion of A. aurita dis- 20 m, 20–40 m and >40 m) in order to resolve the tribution, Table 2). However, significant expansion of extent that a population occurs offshore in comparison the A. aurita distribution away from shore occurred in with isobaths (Fig. 1). Table 2 summarizes results of regions 14, 16 and 17 on the Louisiana shelf. the rank order test of whether frequency of occurrence tends to increase (or decrease) with time either within the entire statistical region or as changes in frequency of occurrence in <20 m or >20 m deep trawl stations. In Table 2, increased frequency of occurrence in the 104

Figure 4. Variations in frequency of occurrence of Chrysaora quinquecirrha in summer SEAMAP trawl collections, 1987–1997 at stations <20 m, 20–40 m and >40 m depth. Depth bins are used as surrogates of distance from shore; refer to Figure 1 for the location of the 20 m and 40 m isobaths within the study regions.

Relationship between summer hypoxia and Chrysaora cies. The extent of summertime hypoxia (stations with quinquecirrha distribution bottom water dissolved oxygen below 2 mg l−1)in the northern Gulf of Mexico over the period of study The relationship between summer hypoxia and sum- is represented in Figures 6 and 7. Figure 6 presents mertime occurrence of Chrysaora quinquecirrha me- the spatial contrast in hypoxia distribution between dusae was explored in Regions 15 and 16 only since the years 1987 and 1997. By 1997, hypoxic bottom these regions have experienced the most consistent waters had extended to a band across the Louisiana change in both distribution and in numbers of this spe- shelf, which coincides with statistical regions 13–17. 105

Figure 5. Variations in frequency of occurrence of Aurelia aurita in summer SEAMAP trawl collections, 1985–1997 at stations <20 m, 20–40 m and >40 m depth. Depth bins are used as surrogates of distance from shore; refer to Figure 1 for the location of the 20 m and 40 m isobaths within the study regions.

Additional patches of hypoxic waters occurred off the Despite the lack of a temporal relationship, there Texas and Alabama coasts but were not as extensive as was substantial spatial overlap between hypoxia and hypoxia on the Louisiana shelf. Though both hypoxia the Chrysaora quinquecirrha medusa distribution on and C. quinquecirrha increased in frequency with time the Louisiana shelf. Mean bottom water oxygen con- during the study period, there is no signiﬁcant correla- centration was compared between stations that did and tion between frequency of occurrence of hypoxia and stations that did not record C. quinquecirrha in trawls. of this species. Over all years, stations that recorded this species in regions 15 and 16 had signiﬁcantly lower dissolved 106

Table 2. Summary of the results of Spearman rank-order analysis of jellyfish distributional shift. Data are presented for the statistical regions identified in Figure 1. Significance within a statistical region indicates that there was a trend toward increased frequency of occurrence with time at stations within or seaward of the 20 m isobath, or over the entire region (overall). 1987–1997 for Chrysaora quinquecirrha; ∗ ∗∗ ∗∗∗ 1985–1997 for Aurelia aurita.( = p<0.05; = p<0.01; = p<0.001; ns = not significant)

Statistical region Chrysaora quinquecirrha Aurelia aurita <20 m >20 m Overall <20 m >20 m Overall ∗∗∗ 11 ns ns ns ∗∗ ∗∗ 13 ns ns ns ns ∗ 14 ns ns ns ns ns ∗∗∗ ∗∗ ∗∗ 15 ns ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ ∗ ∗∗∗ 16 ∗∗ ∗∗∗∗ 17 ns ns ∗∗ ∗ 18 ns ns ns ns 19 ns ns ns ns ns ns 20 ns Ns ns ns ns ns ∗ 21 Ns ns ns ns ns

Figure 7. Variations in the frequency of occurrence of hypoxia and summer Chrysaora quinquecirrha catch in SEAMAP trawls (as per- centage of all stations sampled) in Statistical Regions 15 and 16 only.

Discussion

The fisheries resource survey data used in this study show significant increasing trends in the number and distribution of jellyfish within the northern and northwestern Gulf of Mexico over the past 11–13 years. However, these numerical and distributional trends Figure 6. Distribution of hypoxic bottom waters in summers of were neither uniform nor consistent between regions 1987 and in 1997. Solid circles represent stations where dis- − solved oxygen concentrations were measured below 2 mg l 1;‘x’ and species. Changes in summer Chrysaora quinque- − represents stations where oxygen was measured above 2 mg l 1. cirrha medusae tended to be more in distribution than in abundance, whereas trends involving fall Aurelia aurita medusae tended towards increased numbers, but with little distributional change. Both numerical and distributional changes occurred in the north- oxygen in the lower water column (Student’s T -test, ern Gulf of Mexico, within regions 14–17 on the t = −4.287, p <0.001) (Fig. 8). Louisiana shelf. Chrysaora quinquecirrha showed the 107

ably more sensitive to the effects of eutrophication and overfishing (Caddy, 1993). By contrast, the size of the Gulf of Mexico and openness of its northern shelf waters to exchange makes eutrophication, at least superficially, a dubious explanation for increased jellyfish production. Very large rivers like the Mississippi-Atchafalaya River system, which alone discharges about 90% of the Gulf’s freshwater input, can in fact regulate production rates and patterns on the shelf (Lohrenz et al., 1997). The Mississippi River, like most Gulf estuaries, has greatest discharge rates of freshwater and nutrients during winter and spring and lowest discharge by late summer and fall (Lohrenz et al., 1997). Light Figure 8. Mean and standard deviation of dissolved oxygen concentration in the lower water column at stations (regions 15 and limitation due to turbidity is responsible for a lag in 16) where Chrysaora quinquecirrha was collected in trawls and primary production away from the river mouth (Ran- at stations where C. quinquecirrha was absent in all years. There dall & Day, 1987; Lohrenz et al., 1990). Peak nutrient is a significant difference between the two means (Student’s t-test, utilization by phytoplankton (Lohrenz et al., 1990) and p<0.05). subsequent secondary production (Dagg, 1995; Ortner & Dagg, 1995) occurs well downstream of the dis- greatest change in regions 15 and 16, and A. aur- charge point. This is typically toward the west along ita showed the greatest change in regions 14, 16 and the Louisiana shelf (Wiseman & Garvine, 1995). Al- 17. As such, the following discussion emphasizes the though rapid utilization of nutrients probably occurs changes that have occurred on the Louisiana shelf. within 100 km (Nelson & Dortch, 1996) once suspen- Long-term ecosystem change that favors jellyfish ded sediments are removed through settling (Lohrenz has been the focus of recent discussion since increased et al., 1990), decoupled downstream (i.e. westward) jellyfish production may be symptomatic of degraded effects will continue due to the high organic load ecosystem health (Caddy, 1993; Mills, 1995, 2001; carried by the coastal current. Pauly et al., 1998). While changes in Gulf of Mex- The combined effects of high nutrient loading and ico jellyfish populations over the past 11–13 years are retention of productive water on the shelf to the west of unequivocal, whether these changes reflect a degraded the river mouth makes the Louisiana shelf susceptible ecosystem remains to be determined through future re- to the ecological effects of eutrophication typically ex- search. As a foundation for future jellyfish research in perienced by semi-enclosed seas. Moreover, the high the Gulf of Mexico, it is instructive to discuss several volume of freshwater and nutrient discharge coupled key hypotheses that might individually or collectively with the low residence time of nutrients within shallow explain the long-term trends identified in this paper. Gulf estuaries makes the shelf ecosystem particularly sensitive to long-term land-use changes (Bricker & Increased trophic transfer to jellyfish: effects of Stevenson, 1996; Pennock et al., 1999). In the Mis- coastal eutrophication and overfishing sissippi River, nutrient concentrations have more than doubled in four decades (Bratkovich et al., 1994; Numerical increases of jellyfish as a function of in- Turner & Rabalais, 1994) corresponding with a long- creased trophic transfer can result from independ- term production increase on the shelf (Walsh et al., ent effects of overfishing or eutrophication (Legovic,´ 1989; Müller-Karger et al., 1991; Eadie et al., 1994; 1987) or from their combined, synergistic effects Turner & Rabalais, 1994; Rabalais et al., 1996). (Caddy, 1993). This has happened in the Black Sea An indirect effect of eutrophication on jellyfish where combined effects of eutrophication and severe ecology is the seasonal development of hypoxia in overfishing, working in concert with species inva- the northern Gulf of Mexico. Hypoxic waters with − sions and altered hydrology, have led to an increase dissolved oxygen concentrations < 2mgl 1 appear in the zooplanktivorous ctenophore Mnemiopsis leidyi to favour the distribution of jellies through enhanced (A. Agassiz) (in Kideys, 1994; Shiganova, 1998). ecological interactions with other organisms. These Semi-enclosed seas like the Black Sea are understand- interactions can be manifested as increased jellyfish 108 predation rates (Breitburg et al., 1999) and reduced benthic polyp stages. While both Chrysaora quinque- competition or predation with less hypoxia-tolerant cirrha and Aurelia aurita have polyp stages that are species (reviewed in Purcell et al., 2001). Severe sum- dependent on hard substrate, it cannot be concluded mertime hypoxia in the northern Gulf of Mexico may that local presence of adult medusae reflects local explain, in part, the success of Chrysaora quinque- polyp populations. One enigmatic characteristic of C. cirrha on the Louisiana shelf. Hypoxic bottom waters quinquecirrha in the vicinity of Mobile Bay and the on the Louisiana shelf are a result of seasonally high Mississippi Sound is that large, mature medusae ar- organic loading via particle sinking and high stratifica- rive in large numbers despite the lack of scyphopolyp tion suppressing deep-water oxygenation (Justicetal.,´ populations or the occurrence of ephyrae and young 1993). medusae in the region (Burke, 1975; Johnson et al., The relationship between Chrysaora quinquecir- 2001; Graham, unpublished data). rha and reduced oxygen concentration is not clear The location of Chrysaora quinquecirrha and (Figs 7 and 8). This species overlaps extensively with Aurelia aurita polyp populations remains speculative hypoxic waters, yet there is no significant relationship in the absence of basin-wide benthic surveys; how- between occurrence of hypoxia and its occurrence. It ever, a great deal of hard substrate exists on the Gulf could be concluded, then, that while hypoxia does of Mexico shelf. This includes both contemporary and not appear to cause distribution shifts of C. quinque- ancient natural oyster reef, which Johnson et al. (2001) cirrha, hypoxia potentially creates an advantageous suspect as the source, and artificially placed structures environment promoting its success on the Louisiana such as fixed oil and gas production rigs and artifi- shelf. cial reefs. While natural hard substrate has likely re- The potential interaction between overfishing and mained relatively constant over ecological time scales, jellyfish populations in the Gulf of Mexico is less artificial substrate has increased dramatically in re- clear than for coastal eutrophication, and these two ef- cent decades. On the continental shelf between Texas fects may be difficult to separate. The Gulf of Mexico and Alabama, there are currently about 6000 operat- supports among the highest regional fisheries produc- ing and discontinued oil and gas structures. Most of tion in North America due to nutrient inputs through these structures extend from the seafloor to sea-surface Gulf estuaries (Deegan et al., 1986). This includes the such that polyp populations could thrive in appropri- largest fishery by volume in Gulf menhaden, which ate physical and chemical conditions within the water has production cycles mediated by nutrient inputs column (e.g. away from deleterious effects of low dis- from the Mississippi River (Warlen, 1988). Despite solved oxygen: Condon et al., 2001). Interestingly, the heavy fishing pressure placed on Gulf menhaden, the greatest density of oil and gas structures occurs which may be a zooplanktivorous competitor of jelly- on the Louisiana shelf between statistical regions 13– fish in the northern Gulf of Mexico, there has been 17 (Fig. 1), which coincidentally are the regions of no formal stock assessment to indicate that Gulf men- consistent numerical and distributional change for C. haden are overfished (R. Shipp, pers. comm.). Thus, quinquecirrha and A. aurita medusae. it is not possible in this case to attribute fish removal alone as a cause of enhanced trophic transfer to jelly- Long-term climate variations fish populations as has been suggested by Pauly et al. (1998). Certainly, this is an area of intense interest The 11–13-year changes documented in this study for future research in the Gulf of Mexico since fishing might be a reflection of longer period climate vari- effects are so pervasive to jellyfish dynamics in other ations. Climate oscillations such as the El Niño South- ecosystems (Caddy, 1993; Pauly et al., 1998; Purcell ern Oscillation (ENSO) and the North Atlantic Oscil- & Arai, 2001) and may explain, in part, increased lation (NAO) force large-scale variations in the hydro- jellyfish biomass in other ‘open’ ecosystems like the logical cycle of North America, and consequently the Bering Sea (Brodeur et al., 1999). rate of discharge of freshwater and nutrients into the northern Gulf of Mexico. Large-scale climate fluctu- Expansion of benthic polyp populations ations may serve as a major source of the interannual variability in jellyfish populations of the Gulf of Mex- Changes in medusa populations and distribution in ico as has been identified in the Bering Sea (Brodeur the northern Gulf of Mexico may alternatively re- et al., 1999) and in Narragansett Bay, Rhode Island flect a change in the distribution or production of (Sullivan et al., 2001). 109

The years 1992 and 1993 serve as an example sequence of flooding due to the passage of two major of how jellyfish populations respond to hydrological hurricanes. Hurricane Florence landed on the Missis- changes. In 1992, an unusually dry winter-spring sippi River delta in early September 1988 and Hur- over the eastern half of the United States dramatic- ricane Gilbert – one of the strongest Atlantic storms ally decreased freshwater discharge, and subsequently in recorded history – made landfall 2 weeks later in depressed salinity proximal to the Mississippi River northern Mexico and traveled over southern and cent- and Mobile Bay estuary (Lohrenz et al., 1997; Pen- ral Texas causing widespread flooding. The sudden nock et al., 1999). Consequently, very high primary flooding by these two storms most likely resulted in production occurred close to the discharge point of depressed coastal salinities, primary production and the Mississippi River (Prasad et al., 1995; Lohrenz et trophic transfer to jellyfish. al., 1997). Locally increased primary production and salinities likely allowed the incursion of large num- Future trends in jellyfish populations of the northern bers of Chrysaora quinquecirrha into regions 13 and Gulf of Mexico 14, a distribution much closer to the Mississippi River What might be the long-term prognosis for jellyfish discharge than observed in other non-drought years. population changes across the northern Gulf of Mex- In Chesapeake Bay, production of ephyrae from the ico? Given our current understanding of how jelly- polyp stage is enhanced by food, and is also very fish populations function in coastal ecosystems, this sensitive to salinity regime (Purcell et al., 1999). question is probably best addressed in the context of By contrast, by mid-late summer 1993, the Mis- nutrient loading to the shelf from large river systems. sissippi River experienced record flooding as a result Additional nutrient loadings to the Gulf of Mexico of ‘El Niño’-induced weather patterns. The excessive shelf could enhance jellyfish populations if loading led input of freshwater and nutrients onto the Louisiana to increased secondary production on the shelf and, shelf during the summer 1993 led to the most extens- perhaps, to increased distribution and magnitude of ive hypoxic zone recorded on the shelf in 1993 with hypoxia. Inputs of new dissolved nutrients into the effects that carried into 1994 (Rabalais et al., 1998). northern Gulf of Mexico are linked to the hydrological Depressions in the number and distribution of summer cycle and climate, and if global warming is incorpor- Chrysaora quinquecirrha occurred during the height ated into this scenario nutrient loading to the shelf may of the flooding on the Louisiana shelf (Figs 2 and indeed increase. In a recent study, Justic´ et al. (1997) 4). Fall Aurelia aurita numbers and distributions were modeled a 50% increased in shelf primary production consistently reduced only in 1994, a 1 year lag behind as a function of a 20% increase in Mississippi River the flood. This might suggest that perhaps the flood discharge – a reasonable expectation under current impacted polyp habitat more than it impacted exist- global warming scenarios for the coming decades. An ing medusa populations. Purcell et al. (1999) have additional consequence of this climate change scen- shown experimentally that success of C. quinquecir- ario is the potential expansion and duration of hypoxic rha polyps is strongly tied to salinity regime. Since bottom waters in the northern Gulf of Mexico (Justicet´ climate variations occur at decadal scales or longer, al., 1996). Therefore, if shelf production and hypoxia I cannot at this point resolve their relevance to pop- are in fact driving jellyfish populations, a long-term ulation changes experienced in the past 11–13 years. increase in population numbers may be expected. Climate variations may also play a key role in Gulf circulation such as spin-off eddies from the tropical Loop Current, which may be critical in advection of Summary and conclusions medusae from their origin to adult nearshore habitats (e.g. Johnson et al., 2001). Loop Current spin-off ed- Chrysaora quinquecirrha medusae have increased dies have been implicated in the transport of sporadic both numerically and in breadth of distribution during tropical cubomedusae (Graham, 1998) and large num- summers 1987–1997 in the northern Gulf of Mexico. bers of the rhizostome medusa, Phyllorhiza punctata These increases have occurred in the vicinity of two von Lendenfeld in 2000 (Graham, unpublished data). major river systems: Mobile Bay and the Mississippi– Another source of long-term variability is hur- Atchafalaya River systems. Most importantly, these ricane activity. The depression in Aurelia aurita num- total numerical increases are linked to an offshore bers and distribution in fall 1988 across the western expansion of the population’s distribution. This is es- and northwestern Gulf of Mexico was likely a con- pecially troublesome off the Louisiana and northeast 110

Texas shelf where summertime hypoxia significantly Bricker, S. B. & J. C. Stevenson, 1996. Nutrients in coastal waters: overlaps with the distribution of C. quinquecirrha me- a chronology and synopsis of research. Estuaries 19: 337–341. dusae, and it is predicted that long-term changes in Brodeur, R. D., C. E. Mills, J. E. Overland, G. E. Walters & J. D. Schumacher, 1999. Recent increase in jellyfish biomass in the nutrient loadings may yield greater densities and dis- Bering Sea: possible links to climate change. Fish. Oceanogr. 8: tributions of C. quinquecirrha medusae in the future. 296–306. Aurelia aurita medusae have increased numeric- Burke, W. D., 1975. Pelagic Cnidaria of Mississippi Sound and adjacent waters. Gulf Res. Rep. 5: 23–38. ally within fall collections 1985–1997 to a greater ex- Burke, W. D., 1976. Biology and distribution of the macrocoelen- tent than summer Chrysaora quinquecirrha although terates of Mississippi Sound and adjacent waters. Gulf Res. Rep. these increases typically did not correspond to wide- 5: 17–28. spread change in distribution. Numerical increase and Caddy, J. F., 1993. Toward a comparative evaluation of human impacts on fishery ecosystems of enclosed and semi-enclosed seas. distributional expansion away from shore occurred to- Rev. Fish. Sci. 1: 57–95. gether in three regions located off the mouth of the Condon, R. H., M. B. Decker & J. E. Purcell, 2001, Effects of Mississippi River and the western Louisiana shelf. low dissolved oxygen on survival and asexual reproduction of This paper presents evidence that two species of scyphozoan polyps (Chrysaora quinquecirrha). Hydrobiologia 451 (Dev. Hydrobiol. 155): 89–95. Gulf of Mexico jellyfish have increased both in dis- Dagg, M. J., 1995. Copepod grazing and the fate of phytoplankton tribution and abundance over a 11–13-year period. in the northern Gulf of Mexico. Cont. Shelf Res. 15: 1303–1317. However, beyond the distributional overlap between Dagg, M. J. & T. E. Whitledge, 1991. Concentration of copepod summer Chrysaora quinquecirrha and hypoxia, it is nauplii associated with the nutrient-rich plume of the Mississippi River. Cont. Shelf Res. 11: 1409–1423. not possible to definitively link this ecological change Deegan, L. A., J. W. Day, J. G. Gosselink, A. Yanez-Arancibia, G. to human activity either through coastal fertilization or S. Chavez & P. Sanchez-Gil, 1986. Relationships among phys- through increased habitat availability. Rather, it is sug- ical characteristics, vegetation distribution and fisheries yield in gested that long-term variations in jellyfish abundance the Gulf of Mexico. In Wolfe, D. A. (ed.), Estuarine Variability, Academic Press New York: 83–100. and distribution may be influenced by environmental Eadie, B. J., B. A. McKee, M. B. Lansing, J. A. Robbins, S. Metz & changes. A great deal of additional work is now J. H. Trefry, 1994. Records of nutrient-enhanced coastal ocean needed so that we can understand how jellyfish pop- productivity in sediments from the Louisiana continental shelf. Estuaries 17: 754–765. ulations respond to both natural and human-induced Goy, J., P. Morand & M. Etienne, 1989. Long-term fluctuations modifications of the Gulf of Mexico shelf ecosystem. of Pelagia noctiluca (Cnidaria, Scyphomedusa) in the western Mediterranean Sea. Prediction by climatic variables. Deep-Sea Res. 36: 269–279. Graham, W. M., 1998. First report of Carybdea alata var. grandis Acknowledgements (Reynaud 1830) (Cnidaria: Cubozoa) from the Gulf of Mexico. Gulf Mex. Sci. 16: 28–30. I thank Mr Kenneth Savastano and his staff at the Johnson, D. R., H. M. Perry & W. D. Burke, 2001. Developing jelly- United States National Marine Fisheries Service for fish strategy hypotheses using circulation models. Hydrobiologia 451 (Dev. Hydrobiol. 155): 213–221. providing access to, and assistance with, the SEAMAP Justic,´ D., N. N. 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