Besides ecologically important, the species is a very valuable fisheries resource in the North Sea and various other areas (Adriatic Sea, Black Sea). In the past commercial interest has motivated and still does numerous studies at several levels, from the species individual physiological performance to ecological population dynamics and commercial fisheries. Yet it is amazing that despite being so abundant and so extensively studied, still basic life history features like growth conditions and population regulating mechanisms are still unclear.
The aim of this project was to identify the remaining gaps in knowledge and to try to fill in some of them. As a starting point the synopsis of Tiews (1970) was taken. However, this overview on brown shrimp biology and fisheries was published almost four decades ago. Since then many other relevant investigations were available and the need for an update was felt. Starting from a life cycle perspective, an extensive literature review was then made in Chapter 2. Additionally, a latitudinal perspective was adopted because the species geographic distribution covers a wide area in the European shallow coastal zone, from 34 to 67 LN, with very different environmental conditions.
Surprisingly in several fields almost any progress had been made. Since Tiews (1970) still the taxonomic status of Crangon crangon is unclear. Also, the existence of genetically different European populations could not be excluded and should be clarified by means of molecular tools. Another basic gap in knowledge is the lack of information regarding growth conditions in the field in relation to abiotic and biotic conditions, including the possibility of counter-gradient growth compensation. Already Tiews (1970) observed growth differences between males and females. However, although both sexes can be identified morphologically, in field studies this aspect has been neglected so far. Detailed information on growth would provide insight into the population structure and dynamics of C. crangon over its distributional range and form a starting point for recruitment studies. This would also finally permit an analysis of latitudinal gradients in lifehistory parameters.
To contribute for clarifying the species sub-population structure two approaches were applied: [1] a classic morphometry study, based on the size of certain morphological traits, and [2] a genetic analysis. The same brown shrimp samples were used in both approaches. These were collected at 25 locations across the entire species geographic distribution area; only the White Sea was not cover in these studies.
Previous work in British waters suggested the existence of subpopulation structure already at a small local scale (100 km) based on morphometry. In Chapter 3 we extended the study to cover the whole geographic range of Crangon crangon and test whether the same method could be applied to describe subpopulation structure at a much larger scale (1000 km). The 25 brown shrimp samples provided information on spatial variability in morphometric characters. In addition, at four sites (Bodø, Norway; Wadden Sea, The Netherlands; Minho and Lima estuaries, Portugal) we assessed the temporal variability in morphology.
Morphological differences between major zoogeographical zones enable to clearly distinguish between populations from the Adriatic Sea, Black Sea, Mediterranean Sea and NE Atlantic. However, opposing expectations, at a local scale, subpopulations frequently cannot be identified due to individual variability, reflected in temporal variability. Hence the morphometric approach is inappropriate to distinguish between populations at small scale.
The taxonomic status and the genetic population structure was studied in Chapter 4 by sequencing a 388 bp fragment of the cytochrome-c-oxidase I gene of Crangon crangon for 140 individuals from the same 25 locations across the distribution range of the morphometric study. Also some other Crangon species were analysed: C alaskensis from the coast of Washington State, USA, and Kodiak Island, Alaska, USA; C.septemspinosa from Tuckerton, New Jersey, USA; C. cassiope from Wakasa Bay, Japan and C. amurensis from Tedai Bay, Japan.
Genetic tools provided clear evidences on brown shrimp s strong population structure. Surprisingly, across the entire geographic distribution area, only four major phylogeographic groups could be distinguished: the northeast Atlantic, the western Mediterranean, the Adriatic Sea and the Black Sea. These groups also correspond to well define geographic regions, the same distinguished in the morphometry study, suggesting that gene flow between basins is very restricted. The biogeographic history of the taxon is largely in accordance with the geographic history of its distribution range. The western Mediterranean populations are the oldest and most variable of the four groups. Black Sea and Mediterranean populations are currently disconnected, though colonization of the first happened relatively recently, possibly earlier than 7000 years ago. Remarkably, within the northeast Atlantic, a genetic homogeneity was found from Morocco to Iceland and Baltic Sea which might be resultant to recent colonization, following the glacial cycles of the late Pleistocene, despite restricted gene flow.
The observed genetic subpopulation structure let to the decision to focus the further studies on the northeastern Atlantic population; populations from Mediterranean, Adriatic and Black Seas were considered to be genetically apart. From the review (Chapter 2), the lack of information regarding growth conditions in relation to abiotic and biotic conditions was identified as a second unclear question. In Chapter 5, extensive laboratory experiments were performed on small brown shrimps to study the length growth in relation to water temperature. These experiments were carried out under similar conditions for three populations respectively at the northern (Bodø, Norway), intermediate latitude Wadden Sea, The Netherlands) and southern edge (Minho, Portugal) of the species distributional range to determine whether counter-gradient growth compensation occurred. Crustaceans such as C. crangon do not grow continuously but by periodically shedding the hard exoskeleton in a process called moult or ecdysis. Between consecutive moults size increase is very constrained, therefore the rate of growth is a function of the frequency of moults and depends on two factors: the size increase at a moult (moult increment) and time between moulting periods (intermoult period). Individual growth was followed in order to analyze both components.
Unfortunately, for the Wadden Sea no reliable data could be obtained. As expected, animals from both other populations grew faster at higher temperature. The intermoult period was inversely related to water temperature, while moult increment showed a large variability. Sex and size differences were also found, with males growing slower than females and at a decreasing growth rate with size. However, at the same temperature level, northern shrimps grew faster than southern shrimps, contrasting the thermal gradient expected for the original populations growth would be expected to be slower for the population living at lower temperatures. Therefore, this experimental investigation also suggested compensation in growth counter acting latitudinal thermal gradient.
Population dynamics of Crangon crangon is difficult to assess because reproduction occurs over longer time periods and juveniles emigrate continuously to deeper waters as they grow. To understand the key processes determining recruitment, we must rely on long-term data sets on adults. In Chapter 6, factors influencing fluctuations in C. crangon abundance in the Dutch Wadden Sea were analysed using a long-term dataset from a fyke fishing programme started in 1960. This provided information on adult brown shrimp and several of its predators. C. crangon abundance follows a seasonal pattern with peaks in spring and autumn. Autumn abundance, representing emigration of mature shrimps towards overwintering grounds, is consistently larger (around five times) than spring abundance, which corresponds to the overwintering immigrating of adult shrimps returning to shallow waters. Two hypotheses were tested and discussed: [1] recruits in autumn are related to predator abundance and temperature during previous warmer seasons, and [2] overwintering adults abundance is determined by predation pressure and abiotic conditions in winter. In fact, the predator abundance was the factor most consistently related with shrimp abundance especially in autumn. Autumn abundance was further related to previous winter conditions, while temperature and salinity were relevant factors affecting spring abundance. A significant positive relationship between spring and autumn abundance and annual commercial landings was also found.
The significant positive relationship between spring and autumn abundance and annual commercial landings in the Dutch Wadden Sea (see Chapter 6) reflects the ongoing debate on when these landings originate from. In other words, since reproduction occurs throughout the year, which shrimp generation is the most contributing one to the autumn fisheries peak? On one hand, the position defended by R. Boddeke and colleagues since 1976 was that brown shrimp growth would be fast enough to enable the summer generation to attain commercial size already in the first autumn of life. On the other hand, the argument suggested by B.R. Kuipers and R. Dapper in 1984 was that it is the winter generation the one that sustains the autumn landings by intense settlement during spring. Both arguments are based on different considerations on the species growth: for Boddeke brown shrimp growth should be amazingly fast to enable to reach the commercial size in large numbers within about four months, from summer to autumn; in contrast, for Kuipers and Dapper the species would require at least about nine months till recruiting to fisheries. Therefore, to bring this dispute one step further would require clarification on the growth timeframe from settlement to commercial size. Unfortunately, still no reliable growth data from shrimps in the Wadden Sea are available. Therefore, an alternative was required and for this Dynamic Energy Budgets (DEB) were selected.
Dynamic Energy Budgets can be used to describe the energy flow through individual organisms from the assimilation of food to the utilization for maintenance, growth, development and reproduction. Powerful aspects of DEB theory are that intra- and interspecific differences between species are captured in the same model using only a different set of parameter values and that only 6 parameters are required for predictions on growth and reproduction.
In Chapter 7, the various DEB parameters were estimated based on available information, whereby growth was assumed to be continuous and therefore more or less representing the situation of (continuous) population growth instead of (discontinuous) individual growth. Differences between males and females (maximum size, respectively 7.5 and 9.5 cm total length) were reflected in differences in the fraction of utilized energy spent on somatic maintenance plus growth and the maximum surface area specific assimilation rate.
With the parameters for male and female C. crangon being available, in Chapter 8, the Dynamic Energy Budget theory was applied to predict maximum possible growth in relation to the prevailing water temperature conditions. An upper limit for growth under natural conditions would then be evident. Besides applying the DEB model for the Dutch Wadden Sea population, an extension was made to depict latitudinal trends in the growth timeframe from settlement to commercial size by simulating growth at water temperature conditions at the northern and southern edges of the species distribution. Even though brown shrimp DEB parameters estimates still require an improvement in accuracy, overall the DEB model could be successfully applied.
In the growth trajectory from settlement (around 0.47cm) to fisheries size (around 5.00cm), females do grow faster than males stressing the need of studying sex s trends separately. Maximum growth simulations under optimal food conditions at the Wadden Sea temperature conditions revealed that males would take 1.5 years and females just 1 year from settlement to fisheries size. Therefore, females, which make up the bulk of commercial landings, to become available to the fisheries in autumn, must have settled in the Wadden Sea during the previous autumn, one year before, and hence probably arose from summer generation. Consequently, it is not the summer brood from the current year as Boddeke claimed, nor the previous winter generation as Kuipers and Dapper suggested, but the summer generation from previous year which represents the major contribution to autumn peak in fisheries. The resultant population growth rate must then be much smaller than the one Boddeke purposed and only slightly smaller than the one Kuipers and Dapper estimated. The time required to grow from settlement to fisheries size tends to increase with latitude, with females, taking almost half the time of males. For establishing reliable latitudinal trends in this growth trajectory it would be required the knowledge on settlement and reproduction periods at the distribution edges. Yet this information is scarce since only few studies were conducted in the past at high and low latitude of the species distributional range.
Finally did we make any progress? From the genetics point of view, we did clarify the population structure but it is unknown to what extent new genetic markers can change this perspective. Growth information can be more accurate: we still need field validation and information on maximum growth of brown shrimp from intermediate latitude populations. Also DEB parameters can be more accurate: estimates rely on available datasets on the species biology and improvement of accuracy demands laboratory experiments especially designed for this purpose. Since differences in parameters estimates between individuals from different populations are possible due to environmental variations, ideally in the future the comparisons should be made with a parameters set for each population. DEB model can also be used to reconstruct food conditions in the field. In this case, an accurate age estimation of Crangon crangon is required. An attempt has been made in the past to estimate brown shrimp age counting segments in the outer antenulles and relating with water temperature. This methodology should be tested and validated. Other methodologies such as marking experiments could also be used.
This thesis stresses the need for distinguishing sexes in studies on brown shrimp: faster growth, longer maximum size and maximum age of females, suggest higher mortality of males. This should be further clarified under natural and controlled conditions. Additionally information on reproduction and settlement periods at the edges of brown shrimp distributional range is necessary to confirm the trends observed in DEB simulations for northern and southern populations. The role of the species in the ecosystem functioning requires further studies, namely to clarify to what extent is the brown shrimp dynamics dependent on predation pressure and how important is C. crangon to control their preys populations. Finally, growth simulations applying DEB model at different temperature scenarios might be an important tool to access the impact of global climate change on brown shrimp productivity.