A 25-year study of climatic and density-dependent population

A 25-year study of climatic and density-dependentpopulation regulation of common shrimp Crangon crangon

(Crustacea: Caridea) in the Bristol Channel

P.A. Henderson*, R.M. Seaby and J.R. Somes

Pisces Conservation Ltd, IRC House,The Square, Pennington, Lymington, Hampshire, SO41 8GN, UK.*Corresponding author, e-mail: [email protected]

The results of a 25-year study of the population dynamics of the common shrimp, Crangon crangon, in theBristol Channel are presented.The population size varied seasonally, with maximum abundance occurringin early autumn at the completion of annual recruitment.The number of recruits changed greatly betweenyears, and was positively correlated with both average water temperature from January to August, andriver £ow rate, and negatively correlated with theWinter North Atlantic Oscillation Index. A wide rangeof other physical and biotic variables was found to have no signi¢cant impact on C. crangon abundance. Thepositive relationship between temperature and C. crangon abundance observed for the Atlantic coast duringthis study is the opposite of that found for southern North Sea populations. Similar contradictory responseshave been noted previously for £at¢sh such as sole, Solea solea. This suggests that global variables may act toproduce di¡erent outcomes for Atlantic and North Sea populations of the same species. Over-wintermortality was found to vary with population size so that the adult C. crangon population in spring wasfound to be remarkably stable, and little in£uenced by temperature or other variables. The mortality rateincreased with population size producing clear evidence of density-dependent control. It is suggested thatthis stability is linked to the constant limited availability of suitable habitat, with individuals unable to ¢ndshelter vulnerable to a range of predatory ¢sh. Given the pivotal role of C. crangon within the northernEuropean estuarine ecosystems, this stability may be a critical component for the overall stability of thesystem. A particular feature of this study was the exceptional recruitment observed in October 2002. Thisdid not result in any subsequent increase in adult C. crangon numbers, possibly because there was asynchronous increase in a wide range of predators. While the adult population has remained stable andshowed no temporal trend, there has been an increase in both the average magnitude and between yearvariability in recruitment, which can be related predominately to the recent increase in water tempera-ture. The di⁄culty of predicting the response of this population to continued climate warming isdiscussed. If temperature continues to rise, the present power law describing the increase in recruitmentwith temperature must inevitably break down. If this were to occur, the future trajectory of the C. crangonpopulation could not be predicted, and the continued stability of this ecosystem would no longer beassured.

INTRODUCTION

Common or brown shrimp, Crangon crangon (L.), areamongst the most abundant macro-crustaceans in north-east Atlantic estuaries and shallow bays (Henderson &Holmes, 1987; Hamerlynck et al., 1993; Maes et al., 1998;Hostens, 2000) where they play a key trophic role, feedingupon polychaetes and other small animals, particularlymeiofauna (Pihl & Rosenberg, 1982, 1984; Evans, 1984;Jensen & Jensen, 1985). In Dutch estuarine waters,Hamerlynck et al. (1993) found 80% of all epibenthicindividuals captured to be C. crangon. It is in turn afavoured prey of a wide variety of ¢sh and invertebratesincluding many of great commercial importance(Henderson et al., 1992); Singh & Bromley (1999) notedthat in the central and southern North Sea the meandaily consumption of C. crangon for a whiting weighing150 g was 0.1g. Closely related decapod crustaceans ful¢lthe same key role in other geographical regions, for

example, sand shrimp, C. septemspinosa Say, in NorthAmerica.

Crangon crangon are the subject of a large commercial¢shery in northern European waters (Temming &Damm, 2002). Within Britain, the ¢shery is centred onthe Wash, Thames Basin, Bristol Channel, MorecambeBay and the Solway Firth. Since the 1970s a series ofstudies has reported upon the population dynamics ofC. crangon and the environmental variables that in£uencedtheir recruitment. These studies have tended to emphasizedi¡erent environmental variables. In one of the earliest,Driver (1976) reported on a 30-year time series forMorecambe Bay and noted that the best predictors ofC. crangon landings were salinity and landings in theprevious year. In contrast, Boddeka (1968) showed a nega-tive correlation between February seawater temperatureand the October C. crangon catch o¡ Holland. Attrill et al.(1999) analysed a 12-year time series from the intakes ofWest Thurrock Power Station in the Thames estuary and

J. Mar. Biol. Ass. U.K. (2006), 86, 287^298Printed in the United Kingdom

Journal of the Marine Biological Association of the United Kingdom (2006)

found that C. crangon abundance was correlated todissolved oxygen concentration. Spaargaren (2000)reported on the 40-year time series collected by nettingfrom a beach on the island of Texel, the Netherlands, andfound that annual £uctuations could be explained byvariation in salinity and temperature. Most recently,Siegel et al. (2005) report on a 30-year time series for theGermanWadden Sea.They found that autumn abundancewas negatively correlated to winter water temperature andthe Winter North Atlantic Oscillation Index (WNAOI),and positively correlated with river run-o¡. However,they noted that it was di⁄cult to explain why the responseto the WNAOI was lagged by 18 months, given that themajority of C. crangon only live for one year. In addition tothese large-scale factors, they also found that gadoidpredators could in£uence local abundance. An importantobservation was that no factors were discovered thatcorrelated with spring C. crangon abundance.

The present study of the C. crangon population withinBridgwater Bay in the Bristol Channel adds to our knowl-edge through the analysis of a data set speci¢callycollected to study C. crangon population dynamics. In parti-cular, monthly sampling has been undertaken which givessu⁄cient data to study mortality rates for each recruitmentcohort and identify short-term movements in response toenvironmental conditions. The original motivation for thestudy in 1980 was concern about the decline in C. crangon

abundance expressed by ¢xed-net shrimp ¢shermen afterthe opening of Hinkley Point Nuclear Power Station. Thestudy was initiated because of an acknowledged lack ofunderstanding of the factors determining C. crangon

abundance.Previous studies on C. crangon in the Bristol Channel

undertaken in the 1930s by Lloyd & Yonge (1947), in the1970s by Moore et al. (1979), and the 1980s by Henderson

& Holmes (1987) described their growth, reproductivebiology and seasonal movement, and presented estimatesof the total population size. Together with the morpho-metric study undertaken by Henderson et al. (1990) theknown information all points to the Bristol Channel andSevern estuary as holding a single, self-sustaining, popula-tion. Within the Bristol Channel, C. crangon can live for anumber of years, reproducing ¢rst when about one yearold. There are two peaks in reproductive activity, the ¢rstin January and the second in late spring (Henderson &Holmes, 1987). Newly metamorphosed C. crangon enterBridgwater Bay during the summer and recruitment iscomplete by the autumn. Only a small proportion of thepopulation survives to reach two or more years of age,resulting in a population with the population dynamicscharacteristic of a species that only lives for one year. Thisis similar to the situation found in the Rhone delta (Gelinet al., 2000).

288 P.A. Henderson et al. Population dynamics of Crangon crangon


Figure 1. Monthly time series of common shrimp Crangon crangon abundance in Bridgwater Bay for the years 1981 to 2005. Theabundance is the number of shrimps caught over six hours between high and low water by two of the cooling water pumps atHinkley Point B Nuclear Power Station. The volume of water sampled each month was 3.24�105m3.

Table 1. Statistics comparing Crangon crangon abundancein Bridgwater Bay, Somerset for the 5 year periods 1981^1985and 2000^2004. The abundance is expressed as the number ofC. crangon captured over six hours in a constant volume of3.24�105m3. The time series was adjusted to a standard tidalrange.

Period 1981^1985 2000^2004

Number of observations 61 60Mean 2046 3026Variance 1,125,291 20,372,735Minimum 686 11Maximum 5865 33,901

Over the last 25 years of our study there have beenappreciable changes in climate and the biological commu-nity of Bridgwater Bay. These changes have broadened theresearch objectives to include an understanding of thepotential e¡ects of global warming. The present analysisaddresses the role of both physical and biotic factors indetermining the abundance of C. crangon. In particular,we wished to examine changes in population size and theextent to which the abundance of this key species isconstrained within tight bounds. If climate variation canlead to appreciable changes in C. crangon abundance then

global warming can be anticipated to produce greatchanges in British estuarine communities.

MATERIALS AND METHODS

Fish and crustacean samples were collected from thecooling water ¢lter screens at Hinkley Point B PowerStation, situated on the southern side of the BristolChannel in Somerset, England. The water intakes are infront of a rocky promontory within Bridgwater Bay; tothe east are the 40 km2 Stert mud £ats. The Crangon

crangon were sampled from water varying in depth fromabout 8 to 18m. A full description of the intake con¢gura-tion and sampling methodology is given in Henderson &Holmes (1991) and Henderson & Seaby (1994). Metho-dology has not changed over the 25 years of study. Theseasonal movement of ¢sh and crustaceans within theSevern estuary is described by Claridge et al. (1986),Bamber & Henderson (1994), Henderson & Homes (1991)and Moore et al. (1979). Henderson et al. (1992) give anaccount of the trophic structure within Bridgwater Bay.

Quantitative sampling commenced in 1980 when 24 hsurveys of the diurnal pattern of capture were undertakenin October and November. From these surveys it wasconcluded that samples collected during daylight wererepresentative of the 24 hour catch (Henderson & Holmes,1990), and monthly quantitative sampling commenced inJanuary 1981. The total volume of water sampled permonth, which has not varied over 25 years, is 3.24�105m3.To standardize for tidal in£uence, all sampling dates werechosen for tides halfway between springs and neaps, withsampling commencing at high water (normally about1200 h). The ¢sh and crustaceans were collected hourlyfrom two ¢lter screens for a 6-h period, identi¢ed tospecies, and the number of individuals recorded.

The power station intakes at Hinkley Point are an e¡ec-tive sampler because of their position at the edge of a largeinter-tidal mud£at in an estuary, with extremely powerfultides resulting in suspended solid levels of up to 3 g l71, andlittle light below 50 cm depth. The crustaceans and ¢sh,

Population dynamics of Crangon crangon P.A. Henderson et al. 289


Figure 2. The relationship between Crangon crangon abun-dance and water temperature in January for the years 1981 to2004 inclusive. The trend line is ¢tted by linear regression andthe 95% con¢dence intervals are shown as dotted lines. Nosample was available for January 1986.

Table 2. Analysis of variance for the multiple regression modelrelating log recruitment to the North Atlantic Oscillation, averageriver £ow and average seawater temperature.

DF SS MS F P

Regression 3 1.674 0.558 8.936 50.001Residual 19 1.187 0.0625Total 22 2.861 0.130

Figure 3. The relative size of Crangon crangon recruitment inBridgwater Bay for the years 1981 to 2005. Recruitment ismeasured as the average of the total catch for the Septemberand October samples.

Figure 4. The in£uence of water temperature on Crangon

crangon recruitment in Bridgwater Bay. Relative recruitment isthe average abundance during September and October.Temperature is the average temperature from January toAugust for the same year as the recruitment. The line is ¢ttedby linear regression; the dotted lines are the upper and lower95% con¢dence intervals for the regression line.

pelagic or benthic, are moved towards the intake in thetidal stream, often as they retreat from the inter-tidalzone where they feed. It is likely that they are oftenunable to see or otherwise detect the intake until they aretoo close to make an escape. Light is clearly important foravoidance, because at power station intakes situated inclear water, captures are higher at night (Whitehouse,1986). The e⁄ciency of the sampling method is discussedin Henderson & Holmes (1991). The ¢lter screens have asolid square mesh of 10mm and C. crangon with a carapacelength 411mm are fully retained by the ¢lters, whilesmaller individuals are retained with reduced e⁄ciency(Henderson & Holmes, 1987).

Water temperature and salinity were measured monthlyusing a mercury thermometer and refractometer respec-tively, approximately one hour before low water. Flowmeasured at the Saxon gauge station on the River Severnwas used as a measure of freshwater £ow into the estuary,and records of sunshine, air temperature, wind speed andwind direction were obtained from the UKMeteorologicalO⁄ce. The North Atlantic Oscillation (NAO) indices,calculated as the di¡erence between the normalized sealevel pressure over Gibraltar and the normalized sea levelpressure over south-west Iceland (Jones et al., 1997), wereacquired from http://www.cru.uea.ac.uk/cru/data/nao.htm. While indices for each month and the annualaverage of the monthly indices were tested for their in£u-ence upon C. crangon, it is well known that the NAO isparticularly important in winter, and the NAO winterindex (NAOWI) was calculated as the December toMarch average as suggested by Jones et al. (1997). Theannual position of the Gulf Stream north wall, asexpressed as the 1st Principal component, was obtainedfrom the web site www.pml.ac.uk/gulfstream/inetdat.htm.Data on sunspot numbers were obtained from the SIDCweb site at http://sidc.oma.be/index.php3.

It was not possible to always sample under the sametidal conditions, and the number of C. crangon capturedwas positively correlated with tidal height, becauseC. crangon retreat from the intertidal £ats with the fallingtide and concentrate in the vicinity of the intake. To allowfor tidal di¡erences, the predicted captures were calcu-lated using a linear regression of C. crangon numbers, andtidal range and the tidally adjusted time series calculatedas the di¡erence between the observed and predictedseries, with a constant added to give only positive valuesand a mean abundance approximately equal to that of theoriginal series.

A search using forward and backward multiple linearregression was made for physical and biotic factors corre-lated with the strength of recruitment. Relative annual



Figure 5. Comparison of the observed and predicted recruitment of shrimp, Crangon crangon in Bridgwater Bay. The observed valuesare the mean number sampled in September and October and the predicted were obtained from a multiple regression model with theWinter North Atlantic Oscillation Index, average seawater temperature and average river £ow as the independent variables.

Figure 6. The temporal variation in abundance of adultCrangon crangon in Bridgwater Bay. Relative abundance wascalculated as the average abundance over the months Marchto May inclusive.

recruitment was measured as the average monthly catchfor the months of September and October. The physicalfactors considered were the North Atlantic Oscillationannual average and winter indices, total rainfall, totalriver £ow, average salinity, average seawater temperature,average annual sunspot number, average wind speed andtotal solar insolation. Biotic factors considered were thetotal annual abundance between January and Augustinclusive of: (1) the approximately 80 species of ¢shcaught in the samples; (2) all predatory ¢sh (mostly

gadoids); (3) whiting, Merlangius merlangus; and (4) swim-ming crabs which were predominately Liocarcinus holsatus.

RESULTSLong-term trends in abundance

The 25-year time series of monthly relative abundance ofCrangon crangon in Bridgwater Bay is shown in Figure 1.Thereis a seasonal cycle of abundance, with annual maxima inlate summer/early autumn, when annual recruitment was



Figure 7. Curves showing the decline in abundance of shrimp, Crangon crangon, cohorts for the years 1981 to 1992 in BridgwaterBay. The lines were ¢tted by regression analysis and each graph includes the coe⁄cient of determination (r2) and the gradientwhich is the instantaneous daily rate of mortality (m).

complete, and minima in May following losses over thewinter months. The time series shows a gradual decline inmean abundance between 1981 and 1991 followed by anincrease that has continued until 2005. More notable thanthe trend in abundance is the clear di¡erence in the varia-bility of the series. Since 1994 the series shows a much morepronounced seasonal pattern of abundance with generallyhigher maximum autumnal abundances. Table 1 compares

abundance statistics for the two 5-year periods between1981 and 1985 and 2000 and 2004. There has been anapproximately 50% increase in mean abundance, but thisis not statistically signi¢cant (t¼70.170, df¼119, P¼0.866)because the variance has increased from approximately 106

to 20�106. Much of the increase in mean abundance andvariance is related to a single exceptional burst in abundancein October 2002 (Figure 1).



Figure 8. Curves showing the decline in abundance of shrimp, Crangon crangon, cohorts for the years 1993 to 2004 in BridgwaterBay. The lines were ¢tted by regression analysis and each graph includes the coe⁄cient of determination (r2) and the gradientwhich is the instantaneous daily rate of mortality (m).

Outliers

There have been six occasions when unseasonably extre-mely low or high catches have been recorded.The two lowswere in August 1983 and 1995 when water temperatureswere respectively 22.6 and 238C. These are the only twosampling occasions in the last 25 years when the seawatertemperature exceeded 228C. Unusually high abundanceswere observed in four late summer-autumn samples,September 1988, September 1994, October 2002 andAugust 2003. These peaks in abundance re£ect years withexceptionally good recruitment, which is discussed below.The peak abundance inJanuary 1997 occurred when water

temperature was only 4.58C, and as shown in Figure 2,winter abundance tends to be higher at lower seawatertemperatures (r2¼0.34).

Variation in annual recruitment

The annual abundance of C. crangon reaches a maximumin September or October, and the average abundance overthese months gives an index of the between-year variationin recruitment. As shown in Figure 3 there is considerablebetween-year variation, and recruitment in 2002 wasabout 25 times as large as that observed in 1985. Thereare also indications that recruitment has increasedthrough time, as the average relative recruitment indexfor the years 1981^1993 was 2221 and from 1994 to 2004it was 5322 captured in six hours.

Multiple regression analysis identi¢ed the followingthree factors as statistically signi¢cant predictors of logrecruitment strength: (1) the Winter North AtlanticOscillation Index (WNAOI) for the winter prior torecruitment; (2) average monthly River Severn £ow forthe months of September and October (F) in the year ofrecruitment; and (3) average seawater temperature (T)for the months of January to August in the year of recruit-ment. The regression equation shown below explained ahigh proportion of the total variability in annualrecruitment (Table 2) with an adjusted coe⁄cient ofdetermination of 0.52.

log10(Recruits) ¼

0:587� 0:127WNAOIþ 0:000634Fþ 0:181T

where F is measured in millions of cubic metres per monthandT in degrees centigrade.



Figure 9. The variation in mortality rate with population sizefor shrimp, Crangon crangon in Bridgwater Bay. Population sizeis the peak number of recruits in autumn. Instantaneousmortality rate was calculated using regression analysis. Thestraight line was ¢tted by linear regression.

Figure 10. The variation in predatory ¢sh abundance for Bridgwater Bay between 1981 and 2005. Abundance is expressed as thetotal catch between August and March, which is the period from peak Crangon crangon recruitment to the beginning of C. crangonreproduction. Separate lines are shown for whiting, Merlangius merlangus, and all predatory ¢sh including whiting.



Figure 11. The pattern of annual abundance in ¢sh and crustacean species that showed a marked peak in relative abundance inBridgwater Bay in 2002. (A) Conger conger; (B) Dicentrarchus labrax (L.); (C) Platichthys £esus (L.); (D) Syngnathus rostellatus Nilsson;(E) Solea solea L.; (F) Pomatoschistus minutus (Pallas); (G) Trisopterus luscus (L.); (H) Liocarcinus depurator; (I) Eupagurus bernhardus;(J) Pilumnus hirtellus; (K) Palaemon serratus; (L) Crangon crangon. Data for 2002 are shown as a black bar.

Average seawater temperature showed the largest(r2¼0.60) and most signi¢cant (P50.001) correlation withthe logarithm of recruitment abundance (Figure 4). Figure5 compares the observed and predicted recruitment throughtime.While the model clearly captures the general trend andlevel of the population it failed to predict the extraordinarilylarge recruitment observed in 2002.

Temporal variation in the adult population

In the Bristol Channel Crangon crangon reproduces fromJanuary to July, with the highest proportion of femaleC. crangon (approximately 75% of the female population)carrying eggs in June (Henderson & Holmes, 1987). Theaverage abundance between March and May inclusivegives the best estimate of the relative size of the reprodu-cing population prior to the main reproductive e¡ort.Abundance in July is a less reliable measure, as femaleswith mature eggs leave Bridgwater Bay.

As shown in Figure 6, there is no signi¢cant trend in adultabundance. A comparison of Figure 3 and Figure 6 demon-strates that recruitment in the autumn is considerably morevariable than adult abundance in the spring (recruitmentvaries between years by a factor of almost �25 for recruits,compared with only �4.4 for the adults).

Density-dependent control

Thegeneral stabilityof theC. crangonabundance time series,together with the considerable reduction in temporal varia-bilitybetweenautumnrecruitmentandthe springadultpopu-lation, suggests density-dependent regulation. Bulmer’s testfor density-dependence (Bulmer, 1975) when applied to thetime series of the total number caught per year, indicated thatthe time serieswas signi¢cantly di¡erent froma randomwalk(test statistic R¼71.37�10714, which is less than the 5%signi¢cance value of R¼1.055, N¼24). This test is highlyconservative, as density-dependence would be rejected ifthere hadbeen anydrift or trend inthe data.

Using the monthly abundance estimates, the instanta-neous mortality rate of the recruits over their ¢rst winterwas calculated using linear regression with log10 abun-dance as the dependent and days since 1 August as theindependent variable.

The ¢tted curves for recruitment for the years 1981 to2004 are shown in Figures 7 & 8. In each case theabundance was plotted from the annual peak in recruit-ment in the autumn until May the following year. Theactual month in which the peak occurred varied fromyear to year. The estimated instantaneous mortalityrate, m, varied considerably between years rangingfrom a minimum of 0.0013 d71 in 1992 to a maximumof 0.0171 d71 in 2002. A mortality rate of 0.0256 d71

was estimated for the 1983 cohort, but this is unreliableas the peak in recruitment was not observed untilJanuary (typical peaks were in August or September)and it is likely that the peak re£ected movementwithin the estuary rather than recruitment.The geometricmean mortality rate for all cohorts except 1983 was0.008 d71.

The mortality rate, m, was positively correlated(r¼0.67) with log C. crangon abundance (Figure 9) andcould be approximately expressed by the equation,

Mortality rate ¼

�0:0191þ 0:0079 log(peak abundance),

where peak abundance is the maximum number ofindividuals captured over six hours during autumnsampling.

Predation and the abundance of other species

While the observed over-winter loss rate for Crangon

crangon may be related to both migration and mortality ora combination of the two, a strong candidate explanationfor the observed density dependence is ¢sh predation.Previous studies (Henderson et al., 1992) have establishedthat many of the ¢sh abundant in Bridgwater Bay,including whiting, Merlangius merlangus, pout, Trisopterusluscus, poor cod,Trisopterus minutus, ¢ve-bearded rocklingCiliata mustela, bass, Dicentrarchus labrax and sole, Solea

solea, feed heavily on C. crangon. During the winter period,when C. crangon numbers decline, the gadoids, and whitingin particular, are highly abundant and appreciablemortality must be caused by ¢sh predation. While winterseawater temperature clearly a¡ects C. crangon movementinto Bridgwater Bay, there is no evidence to suggest thatthe loss in abundance between September and May isprimarily caused by migration. The observed winterdecline in abundance is observed throughout the BristolChannel and Severn estuary and there is no other regionof estuarine or shallow water habitat of su⁄cient size orproductivity capable of holding such a large population.If the loss is caused by predation or competition then anincrease in predator/competitor abundance with C. crangon

abundance might be observed. The trend of increasedC. crangon recruitment (Figure 3) is re£ected in an increasein predatory ¢sh numbers between August and March(Figure 10). Over the period of study there has been ageneral tendency for biological activity to change withC. crangon abundance. For example, as shown in Figure 11,the massive eruption in C. crangon numbers observed in2002 coincided with peaks in abundance of 12 othercommon species.

DISCUSSION

For the past 25 years the adult population of Crangoncrangon within Bridgwater Bay has been notably stable (seeFigure 6). However, average C. crangon abundance hasincreased because recruitment has increased with averageseawater temperature.This has resulted in a clear exampleof density-dependent control as the mortality rate ofrecruits over their ¢rst winter increases with recruitment.The most impressive example of the regulatory ability ofthe system was the response to the extraordinarily largerecruitment in 2002 (see Figures 1 & 3). Recruitment inthis year was more than twice as large as that observed inany year since 1980, yet by the following spring, numberswere close to those observed in other years. While thefactors controlling C. crangon numbers cannot bede¢nitively identi¢ed, it is clear that increased C. crangon

abundance is associated with increased predator andcompetitor abundance. The tendency for whiting, themost abundant of the ¢sh predators, to change in



abundance with C. crangon has been previously noted(Henderson & Holmes, 1989).

In Bridgwater Bay, Crangon crangon migrates with therising tide onto the intertidal £ats, which is a normal beha-viour for the species (Hartsuyker, 1966; Al-Adhub &Naylor, 1975). At low water, the population, which wasdispersed over 40 km2 of intertidal £ats, becomes concen-trated within the permanent water of the estuary. Thepredators of this species are also similarly con¢ned and itmust be a time of great vulnerability for C. crangon indivi-duals that cannot ¢nd a place where they can burrow intothe substrate. The striking stability of the adult populationin spring suggests that a ¢xed physical constraint, possiblythe amount of available habitat, is setting an upper limiton the adult population. It is unlikely that top-downcontrol alone could produce such stability, as the abun-dance of predators has varied considerably through time(Figure 10), and there is no correspondence between thepeaks and troughs in predator and C. crangon abundance.The need to utilize inter-tidal mud £ats for feeding isprobably essential, as the subtidal benthic community isgreatly impoverished, because of substrate instabilitylinked to the strong tidal streams. It may be the extentand productivity of these mud £ats that constrains C.

crangon abundance. However, if bottom-up controlthrough food availability were acting we would need toassume that invertebrate productivity did not change withthe rise in average temperature. As this seems unlikely, theavailability of shelter, with predation taking those that areexcluded, is the explanation that best ¢ts the facts.

While the adult population has remained stable,recruitment as measured by abundance in September andOctober has increased with water temperature. Female C.

crangon carry their eggs and move towards the mouth ofthe estuary to release their eggs; larvae are never foundin plankton samples collected in Bridgwater Bay. Theo¡shore movement of ovigerous females is a well-knownbehaviour of the species (Meyer-Waarden & Tiews, 1957;Tiews, 1970). This is almost certainly related to the avail-ability of food, as the high sediment loadings in the Severnestuary and Bristol Channel greatly restrict the density ofboth phyto- and zooplankton (Joint & Pomroy, 1981).Boddeke et al. (1986) found in the southern North Seathat the settlement of postlarval C. crangon in late May^July was linked to the bloom in calanoid copepods, whichare the major food of C. crangon of 10^20mm in length.Crangon crangon do not enter Bridgwater Bay until theyhave metamorphosed into fully formed small C. crangon

that have adopted a more benthic lifestyle (Henderson &Holmes, 1987). The size of recruitment is therefore deter-mined by events outside Bridgwater Bay.

Recruitment in the autumn was found to be correlatedto seawater temperature, the NAOWI and river £ow.These variables are all known to a¡ect the productivityand growth of estuarine animals. The NAOWI is knownto be positively correlated with recent increased abun-dance of both phytoplankton and small copepods in thesouth-western region (Beaugrand & Reid, 2003) and theenhanced growth of sole in Bridgwater Bay is positivelycorrelated to the NAOWI (Henderson & Seaby, 2005).River £ow, and by implication the NAO, were also identi-¢ed as key variables a¡ecting production and sole growthin the Gulf of Lions (Salen-Picard et al., 2002). It is

therefore surprising that C. crangon recruitment is negativelycorrelated with the NAOWI. It would appear thatC. crangon recruitment is higher when copepods and ¢shdo poorly. A negative correlation between C. crangon

recruitment and the NAOWI was also found by Siegel etal. (2005) for the German Wadden Sea, but with an 18-month lag, which is di⁄cult to explain given that mostC. crangon only live for one year in their study area. It isalso notable that, whereas Siegel et al. (2005) found anegative correlation between C. crangon recruitment andwater temperature, we have found a positive correlation.To some extent, contradictory responses to temperaturecan be explained by di¡erences in migration over the lifecycle. Recruitment of the young is positively correlatedwith seawater temperature while winter abundance ofadults shows a negative correlation. Thus, the perceivedrole of temperature will depend on the timing of samplingwithin the annual cycle. The strength of the present studyis based on the use of a monthly sampling interval. Thereare indications that climatic variables do not act toproduce the same trends in North Sea and Atlanticwaters. Henderson & Seaby (2005) also noted a similarcontradiction in the e¡ect of temperature for sole.

The strong density-dependent control acting upon theC. crangon population is demonstrated by the remarkablystable adult population and the positive correlationbetween the instantaneous mortality rate over their ¢rstwinter of life and the size of the population. In this study,the geometric mean mortality rate for all cohorts except1983 was 0.008 d71, which is of a similar magnitudealthough higher than the rate of 0.006 d71 estimated byHenderson & Holmes (1987) over the entire life of acohort. This would be expected as older and largerC. crangon are probably less prone to predation. A similarstability in adult population size was also noted by Siegelet al. (2005) for the GermanWadden Sea.

The simple power law relationship between recruitmentand seawater temperature reported here can only applyover a limited temperature range and we have no indica-tion of the upper temperature at which it will break down.Crangon crangon can certainly live in warmer waters as itsgeographical range lies between 458 and 578N (Tiews,1970), and the Bristol Channel lies between 51 and 51.58N.While higher spring temperatures increase larval develop-ment rates and probably result in reduced mortality, theremust also be an increase in food availability if this is to betranslated into higher recruitment. It is notable that thevariability of the C. crangon population has increased withseawater warming. The temperature response observed inthis study may re£ect particular features within this geo-graphical area and shrimp populations in other areas mayrespond di¡erently to changes in temperature.

Using previous estimates of population size it is possibleto estimate the recent increase in C. crangon standing crop.In June 1981 and November 1983 the population size onthe Stert £ats in Bridgwater Bay was estimated as 3�106

and 5�107 individuals respectively, suggesting a standingcrop that varied between 106 and 108, with an average ofaround 107 individuals (Henderson & Holmes, 1987). Thisrepresents a biomass of about 104 kg wet weight, as theaverage C. crangon weighs approximately 1g. The abun-dance in Bridgwater Bay in October 2002 was about 26times that observed in the early 1980s, suggesting an



increase in standing crop to about 3�108 individuals,weighing 2.6�105 kg. It is notable that this great increasehad little impact on the stability of the system as measuredby continuing species presence. However, the abundanceof shrimp predators has increased. Over the last 25 yearsthe total biomass and species richness of higher animals inthe Bristol Channel has increased and this change must inpart be supported by, and possibly caused by, the increasein C. crangon recruitment.

The present study demonstrates the di⁄culties inpredicting the e¡ects of climate warming on estuarinecommunities. If temperature were to £uctuate within therange experienced over the last 25 years a remarkablye¡ective predictive model could be produced to describethe change in recruitment with temperature, the tempera-ture-related winter migrations and the density-dependentcontrol on adult numbers. However, recruitment presentlyincreases as a power of the temperature and this relation-ship must break down if temperature continues to increase.It is notable that abundance is low when seawatertemperature exceeds 228C, indicating that C. crangon

avoids the highest temperatures presently experienced. Itis possible to envisage both stabilizing and catastrophicchanges if temperature should increase further. The mostbenign possibility would be that C. crangon recruitmentgradually decelerates with further temperature rises, aswarm water species enter the system and compete forresources. The predators would respond by wideningtheir feeding niches and the ecosystem would gentlyevolve to a higher diversity system more similar to thatobserved in Portuguese estuaries (Costa, 1988). The cata-strophic scenario is that C. crangon recruitment will initiallycontinue to increase with increasing temperature, until apoint is reached at which recruitment fails. This mightlead to a break down in the present density-dependentcontrol as predation pressure intensi¢es, resulting in afurther decline in C. crangon recruitment. If such laggedresponses are important then the system may passthrough a period of high instability before ¢nding a newequilibrium.While further research is required before thee¡ects of climate warming can be predicted, the responseof C. crangon to temperature makes it clear that majorchanges will occur should temperatures continue to rise.

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Submitted 20 April 2005. Accepted 30 January 2006.



A 25-year study of climatic and density-dependent population

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