Universidade de Aveiro Departamento de Biologia 2011
Fabiana Encarna¸
c˜
ao
Pinto Freitas
Populations dynamics of Crangon crangon :
latitudinal comparative study
Dinˆ
amica populacional de Crangon crangon :
um estudo comparativo latitudinal
Universidade de Aveiro Departamento de Biologia 2011
Fabiana Encarna¸
c˜
ao
Pinto Freitas
Populations dynamics of Crangon crangon :
latitudinal comparative study
Dinˆ
amica populacional de Crangon crangon :
um estudo comparativo latitudinal
Disserta¸c˜ao apresentada `a Universidade de Aveiro para cumprimento dos re-quesitos necess´arios `a obten¸c˜ao do grau de Mestre em Biologia Aplicada, no Ramo de Ecologia, Biodiversidade e Gest˜ao de Ecossistemas, realizada sob a orienta¸c˜ao cient´ıfica do Doutor Ant´onio Jos´e Ars´enia Nogueira, Professor Associado com Agrega¸c˜ao, do Departamento de Biologia da Universidade de Aveiro e co-orienta¸c˜ao da Doutora Joana Costa Vilhena de Bessa Campos, Investigadora em P´os-Doutoramento do CIIMAR - Centro Interdisciplinar de Investiga¸c˜ao Marinha e Ambiental da Universidade do Porto e do Doutor Manuel Ramiro Dias Pastorinho, Investigador em P´os-Doutoramento do CESAM - Center of Environmental and Marine studies da Universidade de Aveiro
This work was supported by a grant from Iceland, Liechtenstein and Norway through the EEA Financial Mechanism and the Norwegian Financial Mechanism
o j´uri / the jury
presidente / president Prof. Doutor Jo˜ao Ant´onio de Almeida Serˆodio
Professor Auxiliar, Departamento de Biologia da Universidade de Aveiro (por
del-ega¸c˜ao da Reitora da Universidade de Aveiro)
Prof. Doutor Ant´onio Jos´e Ars´enia Nogueira
Professor Associado com Agrega¸c˜ao, Departamento de Biologia da Universidade
de Aveiro (orientador)
Doutora Joana Costa Vilhena de Bessa Campos
Investigadora em P´os-Doutoramento, CIIMAR - Centro Interdisciplinar de
Inves-tiga¸c˜ao Marinha e Ambiental (co-orientador)
Doutor Manuel Ramiro Dias Pastorinho
Investigador em P´os-Doutoramento, Departamento de Biologia e CESAM - Centre
for environmental and marine studies da Universidade de Aveiro (co-orientador)
Doutor Jos´e Carlos Antunes
Investigador do CIIMAR - Centro Interdisciplinar de Investiga¸c˜ao Marinha e
agradecimentos / acknowledgements
Desejo agradecer as pessoas que contribu´ıram para a realiza¸c˜ao deste trabalho.
Em primeiro lugar agrade¸co ao Doutor Ant´onio Nogueira, na forma como orientou o meu trabalho, pelo tempo que generosamente me dedicou e pela transmiss˜ao de conhecimentos. Seguidamente, gostaria de destacar a Doutora Joana Campos, pela experiˆencia de trabalhar no CIIMAR e por sempre me ter facilitado todas as condi¸c˜oes para desenvolver este trabalho; e o Doutor Ramiro Pastorinho pelas valiosas sugest˜oes e revis˜ao da disserta¸c˜ao.
Gostaria de agradecer ao Doutor Carlos Antunes por disponibilizar todos os meios necess´arios do Aquamuseu para as amostragens no Rio Minho, em especial quero agradecer ao t´ecnico Eduardo Martins pela ajuda no trabalho de campo e a todo o pessoal que trabalha neste instituto pela simpatia e amizade com que sempre nos receberam.
Devo um sincero agradecimento a Silvia Santos, Jeremy Smith, Cindy Pedrosa pelo excelente trabalho nas amostagens e tratamento das amostras do estu´ario de Valosen, na Noruega. Sem esquecer o Doutor Stig Skreslet, Doutor Henk W. van der Veer e Doutora Vˆania Freitas pela sua contibui¸c˜ao na organiza¸c˜ao e coordena¸c˜ao do programa de amostragens. Quero agradecer a todos os meus colegas de laborat´orio do CIIMAR. Principalmente aos alunos de doutoramento Allan Souza e Ester Dias que foram respons´aveis pelo programa de amostragens no Rio Minho, em Portugal. Um especial agradecimento ao Allan Souza que sempre se disponibilizou a me ajudar no que foi necess´ario.
Um bem-haja para Martina Illari, Rita Guillot e Rute Pinto pela amizade e por tornarem as horas de laborat´orio muito mais descontra´ıdas.
Um agradecimento muito especial a Tim van Nus, pelo encoraja-mento e incentivo durante todo o per´ıodo de execu¸c˜ao da tese.
Finalmente, gostaria de expressar a minha gratid˜ao aos meus pais, Helena e Jos´e Freitas, pelo apoio incondicional.
Palavras-chave Altera¸c˜oes clim´aticas, Ecologia Estuarina, Crangon crangon, Dinˆamica pop-ulacional, Produ¸c˜ao secund´aria
Resumo Foram analisadas popula¸c˜oes de Crangon crangon pr´oximas do limite lat-itudinal sul e norte na linha costeira da Europa. Este estudo compreende dinˆamica populacional e productividade da popula¸c˜ao no estu´ario do Minho (NO da Pen´ınsula Ib´erica) e no estu´ario de Valosen (N da Noruega). As popula¸c˜oes foram analisadas mediante a influˆencia dos factores abi´oticos, principalmente temperatura, salinidade, e caracter´ısticas do estu´ario. Uma compara¸c˜ao entre as duas popula¸c˜oes foi realizada, tendo em considera¸c˜ao gradientes latitudinais, processos intr´ınsecos de adapta¸c˜ao da esp´ecie, e as suas respostas a altera¸c˜oes no ecossistema em pequenas escalas de tempo. Este estudo teve em foco os processos de adapta¸c˜ao a locais menos favor´aveis de esp´ecies abundantes, tendo como objectivo a melhor com-preens˜ao na produ¸c˜ao estuarina e fun¸c˜ao ecol´ogica para esta esp´ecie. De facto, o conhecimento das caracter´ısticas estuarinas locais, na sua fun¸c˜ao ecol´ogica, popula¸c˜oes que suportam e suas caracter´ısticas f´ısicas espec´ıficas, podem providenciar dados para pol´ıticas de gest˜ao, para conten¸c˜ao de im-pactos presentes e futuros, resultantes da press˜ao antropog´enica, tais como, altera¸c˜oes clim´aticas globais.
Key-words Climatic changes, Estuarine Ecology, Crangon crangon, Population dynam-ics, Secondary Production
Abstract Crangon crangon estuarine populations were analyzed in the European coast line near the south and northern edges of its latitudinal range. This study comprises a population dynamics and productivity examination on Minho Estuary (NW of the Iberia Peninsula) and on Valosen Estuary (N coast of Norway). The populations were examined on the influence of abiotic factors, foci in temperature, salinity, and estuarine characteristics. A com-prehensive comparison among both populations was performed, including latitudinal trends, species intrinsic processes of adaptation and their re-sponses to ecosystem changes in short time scales. This study, focused on the processes underlying adaptations to less favorable locations of abundant species, aims to contribute to a better understanding of estuarine produc-tivity and the ecological role for this species. In fact, the knowledge of a specific estuary functioning, its ecological role, populations sustained and physical characteristics, can provide reliable data for management polices targeting ongoing and future impacts from anthropogenic pressure, such as, the global climatic changes.
Contents
1 Introduction 1
2 General Review 3
3 Methodology 11
4 Results 17
4.1 Minho Estuary, northwest of the Iberian Peninsula . . . 17 4.2 Valosen Estuary, north of Norway . . . 27
5 Discussion 37
6 Final Conclusions 45
7 References 47
Appendices 59
List of Figures
3.1 Location of the sampled estuaries: Valosen Estuary, Norway and Minho Estu-ary, Portugal . . . 12 3.2 Map showing the location of the sampling stations in Minho Estuary, Portugal 14 3.3 Map showing the location of the sampling stations in Valosen Estuary, Norway 15 4.1 Principal Components Analyses (PCA) analysis for environmental variables
differences for Minho Estuary, Portugal . . . 18 4.2 Crangon crangon densities variations during the sampling period in Minho
Estuary, Portugal . . . 20 4.3 Spatial and temporal variations on Crangon crangon densities for the abiotic
factors, temperature and salinity, in Minho Estuary, Portugal . . . 22 4.4 Canonical Correspondence Analyses (CCA) analysis for Crangon crangon
pop-ulation densities in Minho Estuary, Portugal . . . 23 4.5 Sex-ratio and juveniles total abundance of Crangon crangon in Minho Estuary,
Portugal . . . 24 4.6 Size structure from catches of Crangon crangon in Minho Estuary, Portugal . 24 4.7 Total length biomass relation of Crangon crangon in Minho Estuary, Portugal 25 4.8 Crangon crangon modal class analysis in Minho Estuary, Portugal . . . 26 4.9 Temperatures measured during the sampling period in Valosen Estuary, Norway 27 4.10 Crangon crangon densities variations during the sampling period, in Valosen
Estuary, Norway . . . 29 4.11 Crangon crangon bearing females size distribution in Valosen Estuary, Norway 30 4.12 Sex ratio and juveniles density of Crangon crangon in Valosen Estuary, Norway 31 4.13 Population size distribution from catches of Crangon crangon in Valosen
Es-tuary, Norway . . . 33 4.14 Total length biomass relation of Crangon crangon in Valosen Estuary, Norway 34 4.15 Crangon crangon modal class analysis in Valosen Estuary, Norway . . . 35 E.1 Linear regressions for total length and biomass relation for males and females
of Crangon crangon in Minho Estuary, Portugal . . . 69 H.1 Salinity values for tidal cycles of neap tides in Valosen Estuary, Norway . . . 80
List of Tables
4.1 Mean values and standard deviation for Crangon crangon densities in the sam-pling stations in Minho Estuary, Portugal . . . 21 4.2 ANCOVA results for total length - biomass relationship on the linear regression
lines for Minho Estuary, Portugal . . . 26 4.3 Mean values and standard deviation for Crangon crangon densities in the
sam-pling stations in Valosen Estuary, Norway . . . 31 4.4 ANCOVA results for total length - biomass relationship on the linear regression
lines for Valosen Estuary, Norway . . . 35 A.1 Abiotic factors sampled in situ in Minho Estuary, Portugal . . . 62 B.1 Kruskal-Wallis test results for environmental data of Minho Estuary, Portugal 63 C.1 One-way ANOVA results for density variations in Minho Estuary, Portugal . 65 D.1 Tukey post-hoc test results for density variations in Minho Estuary, Portugal 66 E.1 Overall regression equations for individual biomass and total length, for total
individuals within each month, in Minho Estuary, Portugal . . . 67 E.2 Tukey post-hoc analysis for total lenght-biomass linear regression relation of
Crangon crangon in Minho Estuary, Portugal . . . 70 F.1 Growth and elimination production for each cohort of Crangon crangon in
Minho Estuary, Portugal . . . 71 G.1 Annual growth and elimination production and production and elimination
ratio for Minho Estuary, Portugal . . . 77 I.1 One-way ANOVA results for densities variations among sampled years in
Val-osen Estuary, Norway . . . 81 I.2 One-way ANOVA results for density variations in the year 2005, in Valosen
Estuary, Norway . . . 82 I.3 One-way ANOVA results for density variations in the year 2006, in Valosen
Estuary, Norway . . . 83 v
J.2 Tukey post-hoc test results for density variations for the year 2006, in Valosen Estuary, Norway . . . 85 K.1 Overall regression equations for individual biomass and total length relation,
for total individuals within each month, Valosen Estuary, Norway . . . 87 K.2 Tukey post-hoc analysis for total lenght-biomass linear regression relation of
Crangon crangon in Valosen Estuary, Norway . . . 89 L.1 Growth and elimination production for each cohort of Crangon crangon in
Valosen Estuary, Norway . . . 90 M.1 Annual growth and elimination production and production and elimination
ratio for Valosen Estuary, Norway . . . 97
CHAPTER
1
Introduction
The brown shrimp, Crangon crangon (L.) (Crustacea: Crangonidae), is one of the most abundant epibenthic crustaceans of shallow coastal ecosystems throughout the north-western European coast to the Mediterranean Sea (Campos and van der Veer 2008). Brown shrimp has been referred to as being an important organism in the ecosystem that it inhabits, playing a key role in trophic webs with top-down impacts (ICES 2011; Jensen and Jensen, 1985; Janke 1999 in Jung 2007; Gibson et al. 1995; van der Veer and Bergman 1987; van der Veer et al. 1998). However, it is still unclear whether the population dynamics of the species is subjected to top-down or bottom-up control (Campos and van der Veer 2008). The high densities of this species in the North Sea (averaging 400 ind 100 m−2) (Beyst et al. 2001) support a profitable fishery that can exceed 35,000 ton per year (ICES 2011). As a result of the species’ profitability, the majority of the scientific studies have been conducted within its central European range (Beukema 1992; Kuipers and Dapper 1981), some of these being related to fisheries’ sustainability and impacts (Catchpole et al. 2008; Graham 2003; Lancaster and Frid 2002; Revill and Holst 2004). C. crangon from the southern European coast remain less studied. However, recent efforts were made in Portugal (Campos 2009; Viegas et al. 2007; Viegas et al. 2011), the Mediterranean Sea (Gelin et al. 2000) and the Black Sea (Bilgin et al. 2008).
Differences in species’ population characteristics across their latitudinal range have been the subject for several studies (Brown et al. 1996). However, in 2005, a review of the total number of studies that concern the range margins (382) showed that aquatic and marine systems were less studied, representing only 4 and 5% (Hampe and Petit 2005), respectively. Therefore, little knowledge exists on estuarine populations. With the knowledge that modern climatic change is rearranging geographic distribution of species world-wide (Parmesan and
Yohe 2003) and as the climatic effects are more likely to be first expressed in estuarine systems (Beukema and Dekker 2005, Lawrence and Soame 2004, Short and Neckles 1999, Simas et al. 2001) it has become important to study estuarine populations at the limits of their latitudinal distribution, assessing individual growth, population recruitment, abundances and annual and secondary production, since these physiological characteristics can be sensitive to environmental changes (Cabral et al. 2001). Furthermore, the understanding on how populations can adapt to different ecosystems and its variability of physiology and ecological behaviour, can be an important tool for modelling impacts of climatic changes across the European coast, using a common abundant species for biological monitoring (Harley et al. 2006).
This work focuses on the C. crangon population near the edges of its distribution, in the species’ southern and most northern range. It provides a description of population dynamics, population structure, individual growth, secondary and annual production, and population growth trends for this species on two locations in the European coast. Minho estuary, located in the NW of the Iberian Peninsula, lies near the southern distribution limit of C. crangon, which is located further south at the western coast of Morocco (Campos and van der Veer 2008). Valosen estuary is located in the north of Norway, close to the northern distribution limit of the species. In both estuaries, brown shrimp is one of the most abundant species. Furthermore, these ecosystems share common epibenthic species, for example green crab (Carcinus maenas), gobies (Pomatochistus sp.) and flatfishes (Costa-Dias et al. 2010; Freitas et al. 2010). Concerning human impacts, Minho estuary is considered an ecosystem with low anthropogenic pressure and contamination levels (Moreira et al. 2006; Reis et al. 2009) and the Valosen estuary has a low human population density in the surrounding areas (Statistics Norway, 2011), however, to the authors’ best knowledge, no study concerning contamination levels was ever conducted.
The aim of this study is to obtain a better understanding of C. crangon population characteristics on the margins of its range and to provide useful data for future comparison studies. This study also contributes to the knowledge of brown shrimp population dynamics within relatively undisturbed ecosystems.
Thesis outline
This thesis comprises: a general review of anthropogenic impacts on estuaries, C. crangon population characteristics (Chapter 2); a methodology for both estuaries (Chapter 3); the analyses of C. crangon population dynamics in Minho and Valosen estuaries, on the level of spatial and seasonal distribution and population traits (Chapter 4); a discussion on the main characteristics of the two population (Chapter 5); and final conclusions (Chapter 6).
CHAPTER
2
General Review
Estuaries and anthropogenic impacts
Estuaries have been supporting human activities since prehistoric times, with centuries of overexploitation, habitat transformation and contamination, subjected to high anthropic pressure due to their high productivity and high economic value. In fact, these ecosystems improved development and supported most of our wealthiest civilizations (Lotze 2007; Lotze et al. 2006). As a result, human impacts pushed estuarine and coastal ecosystems away from their historical status of rich, diverse and productive ecosystems (Kennish 2002; Lotze et al. 2006). Several examples of physical degradation and depletion of natural resources are known throughout history (see Lotze et al. 2006), with numerous fishery collapses and food web changes (Jackson et al. 2001; Lotze 2005, 2007; Lotze and Milewski 2004). Ad-ditional anthropogenic impacts in estuaries consist of the industrialization and agricultural exploitation, increasing quantities of human waste (causing high eutrophication that leads to the nuisance of several toxic algae proliferation) and physical destruction by infrastructure constructions, for commercial and/or habitation purposes (Hallegraeff 1993; Kennish 2002; Nixon 1995). Despite, the majority of the estuaries are already impacted by anthropogenic activities. Future prediction points out that by the year of 2025 estuaries will be severely impacted by habitat loss due to human activities, mainly related to the increase of human populations in coastal areas, which are estimated to reach six billions (Kennish 2002).
Human’ domination is leading to major changes in landscape, biological mechanisms and cycles world wide, through depletion of resources, high rates of contamination, physi-cal changes and climate changes (Kennish 2002; Lotze et al. 2006; Vitousek et al. 1997). Global climate change is now accepted as a factor that challenges the preservation of hu-man settlements, commercial interests and cultural traditions, by, for instants, population
displacement (Lonergan 1998) specially from coastal zones (McGranahan et al. 2007), im-pacts on food and water supplies (Arnell 1999; Parry and Swaminathan 1992; Rosenzweig and Parry 1994; V¨or¨osmarty et al. 2000), dramatic impacts on human social systems (Barnett and Adger 2007) and increasing occurrence of diseases (McMichael et al. 2006).
In addition, estuaries may be the habitats where climatic effects are first expressed. Sea level rise and changes in river flow will alter the sediment balance in estuaries, resulting in changes in the environmental conditions for organisms that form permanent local communities or use estuaries as temporary habitats (Beukema and Dekker 2005; Lawrence and Soame 2004; Short and Neckles 1999; Simas et al. 2001). Due to the important role played by estuarine ecosystems, the current anthropogenic impacts and trend of human population increase, an effective management of these systems has become vital (Costanza et al. 1997; Vitousek 1994). This can only be achieved with the understanding on how these ecosystems function-, including knowledge of species’ reproductive cycles, juvenile nurseries and the ongoing human exploitation of biological and ecological resources. This requires a proper study of the complex estuarine ecosystem, including the identification of species that perform key functions and the understanding of food webs (Beck et al. 2001). Despite the existence of analytic models in marine ecology, there is still a need for knowledge on how to apply these on local conditions for a better support of fair management policies (Costanza et al. 1993).
Crangon crangon, the brown shrimp
Crangon crangon, vernacularly known as the brown shrimp, is an abundant decapoda crustacean that inhabits shallow coastal and estuarine waters, ranging from the northwestern edge in Iceland up to Norway, including the coast of Ireland, United Kingdom, and the northern coast of Europe. Its range extends in southern direction to the western coast of Morocco, with populations throughout the Mediterranean and Black Sea (Campos and van der Veer 2008; Holthuis 1980). According to Luttikhuizen et al. (2008), within the species range four major groups were identified: the northeast Atlantic (including Baltic Sea), the western Mediterranean, the Adriatic Sea and Black Sea. In this study, the authors refer to a restricted gene flow between these groups, due to physical barriers formed by the Strait of Gibraltar and the Oran Almeria front, the Sicilian Straits and the Turkish Strait. In fact, little genetic flow had been described for some widespread marine population of invertebrates and fish, along the southeast coast of the USA (Avise 1992, 1994) and in mussels from French and Spanish coasts in the Mediterranean Sea (Sanjuan et al. 1996). Also, a genetic cline was observed between each side of the strait of Gibraltar, for the majority of fish and invertebrate species analysed by Borsa et al. (1997). Despite the gene flow restriction that could exist among C. crangon populations, the current invasion rates by ballast waters should be considered (Streftaris et al. 2005). This pathway is responsible for transporting viable larvae into other locations; in C. crangon it was proven effective with the colonization of
5
Iceland’s coastal waters (Gunnarsson et al. 2007; Streftaris et al. 2005).
The wide latitudinal distribution range (34 to 67°N), infers a high resilience and plasticity of the species to temperature ranges, as well as to highly diverse coastal ecosystems. The case of Iceland’ s rapid colonization can be, again, cited to illustrate the species’ adaptability. It was first detected in 2003, and by the year 2006 it had colonized most of the suitable habitats in the west and south coasts, reaching values up to 6,700 ind 100 m−2 (Gunnarsson et al. 2007).
The brown shrimp inhabits soft bottoms in estuarine and shallow coastal waters. It has a preference for fine sediments, from muddy to sandy substrate (125 to 710 µm) (Pinn and Ansell 1993), and depths from 0 - 20 m, with some records up till 130 m (Holthuis 1980). As a euryhaline species (Broekema 1978; Criales and Anger 1986; Lloyd and Yonge 1947; Tiews 1970) it occurs at salinity values from close to 0 up to 35 (Mouny et al. 2000), being com-monly found in waters of low salinity of 1 - 5 (Boddeke 1976; Havinga 1930). Its temperature tolerance ranges from 6 to 30°C (Jeffery and Revill 2002; Lloyd and Yonge 1947). However, at low temperatures, C. crangon shows migration towards higher salinities in offshore waters (Broekema 1978).
Life cycle
Migratory movements also occur during reproduction, as individuals move towards off-shore, more saline waters into depths between 10 to 20 m (Henderson and Holmes 1987; Tiews 1954). In fact, successful development of eggs depends on salinity and temperature, as with salinity values below 15, eggs are unable to develop. With higher temperatures egg develop-ment can occur at lower salinities (Broekema 1942; Gellin et al. 2001). The developdevelop-ment of viable eggs occurs between 6-21°C (Wear 1974) and incubation time mainly depends on this parameter (Meredith 1952; Tiews 1954). Differences in conditions for eggs incubation was already described by various authors (summarized in Temming and Damm 2002), and accord-ing to their results, the full egg development, varies from 2-3 weeks at 20°C, to three months at 6°C (Campos and van der Veer 2008; Kuipers and Dapper 198). C. crangon reproduction was extensively described by Lloyd and Yonge (1947) and Boddeke et al (1991). Previously, Tiews (1970) stated for an external fertilization for these shrimps. Further on, Boddeke et al. (1991) suggested that this species had internal fertilization: males apparently transfer their sexual products directly from their gonopores into the oviducts of females, resulting in the internal fertilization of the eggs. This process, as far as it is known, remains an exception among all the Caridae species (Correa and Thiel 2003). After copulation, the moment of spawning varies according to the size of the female; it occurs instantly for small individuals, 24 h for larger and 48 h for the largest individuals. After the egg’s extrusion, females provide parental care by carrying them stuck to their pleopods, attached with a post-spawning
secre-tion (Lloyd and Yonge 1947). The reproductive season, at intermediate latitudes, generally ranges from January to September, with two discrete peaks: one in winter/early spring (the winter brood; ranging from January to June) and another in summer (the summer brood; ranging from July to September) (Oh and Hartnoll 2004; Temming and Damm 2002). A sequence of spawning was determined according to individual size. For example, in the Baltic Sea, larger sized shrimps begin to spawn earlier than the smaller ones. As of May, egg-bearing shrimp size ranged between 50 to 60 mm, whereas only from June onward, smaller bearing females were reported, starting at 30 mm of total length (Henking 1927, in Tiews 1970). In addition, compared to summer season, winter eggs and hatched-larvae are larger and these larvae are more resistant to starvation (Boddeke 1982; Paschke et al. 2004).
Hatched larvae are planktonic free-floating, measuring around 2 mm and undergo several pelagic stages (five to six) and a post-larvae stage (Criales and Anger 1986; Gurney 1982). Successful larvae development is dependent on the temperature and salinity conditions, which should range from 9 to 18°C and 32 (i.e. polyhaline conditions), respectively. First stages occur in high salinity conditions, with larvae mortality observed below salinity values of 16 (Criales and Anger 1986). At the end of the last larval stage, in the first or second post-larvae stage, C. crangon averages 4.6 to 4.7 mm in size, and settlement takes place into shallow nursery areas. The development from the first larvae stage to settlement stage takes in average two to five months (Beukema 1992; Boddeke 1976; Kuipers and Dapper 1984; Lloyd and Yonge 1947; Tiews 1970). The process triggering settlement remains unclear. However, in the German Bight larvae transportation from offshore waters to estuarine bottoms seems to be better explained by the combination of tidal currents and the larvae’s vertical movements in the water column (Daewel et al. 2011). Optimum juvenile growth occurs in temperatures around 25°C. Compared to adults, juveniles grow faster, are more tolerant to higher temperatures and prefer lower salinities (Freitas et al. 2007; van Lissa 1977 in Campos and van der Veer 2008).
Sexual maturation normally occurs within the first year of life. In females sexual mat-uration is evident with the presence of eggs, but for males matmat-uration is more difficult to determinate. Even so, values of total length indicating maturity have been established for males of 22 - 43 mm and for females about 30 - 55 mm (Lloyd and Yonge 1947; Oh and Hart-noll 2004). Attaining a mature stage in C. crangon seems to be more related to temperature than to age itself (Meredith 1952).
The brown shrimp has been considered a protandric hermaphrodite species (Boddeke 1965). However, no reliable evidence was shown for sex reversal from males to females, in the rearing experiments of Tiews (1954), Meixner (1970), Martens and Redant (1986) or Schatte and Saborowski (2006) nor on wild population analyses by Siegel et al. (2008). The species’ protandric characteristic has been used to explain the higher abundance of females in groups of larger sized individuals (Boddeke 1965). According to Siegel et al. (2008), this sex
7
change is possible to occur on wild populations. However, it was considered to be a negligible phenomenon for variations on the population’s sex-ratio. In this study, males were dominant in the smaller size classes and if sex change was excluded, the presence of large sized females within a population could be explained by the faster growth rate of females and the males’ shorter life span (Henderson and Holmes 1987; Siegel et al. 2008; Tiews 1970).
Population fluctuations
Population fluctuations can be related to seasonal temperature variations and to predation rates (Oh et al. 1999). C. crangon is consistently abundant throughout its range, therefore its recruitment must be successful in most years and locations (Kuipers and Dapper 1984; Oh et al. 1999; Pihl and Rosenberg 1984; Tiews 1970). However, the processes that explain the relation between the recruitment of juveniles and the adult stock are not fully understood. Species recruitment is dependent on many factors, food availability (Beukema 1992; Broekema 1942; Lloyd and Yonge 1947), predation pressure (Cattrijsse et al. 1997), environmental conditions, e.g., temperature (Boddeke 1976; Cowx et al. 1998; Havinga 1930; Kuipers and Dapper 1984), salinity (Broekema 1942, Henderson and Holmes 1987, Spaargaren 2000), light intensity or photoperiod (Spaargaren 2000) and dissolved oxygen (Attrill et al. 1999).
In a 25-year study in the Bristol Channel (United Kingdom), the recruitment of juveniles was positively related to water temperature and river flow rate, with negative correlations to WNAOI (Henderson et al. 2006). In fact, the juveniles’ abundance can be directly related with water temperature, as this factor can trigger timing of larvae immigration and settlement (Beukema 1992). In juveniles, predation and cannibalism could be important factors for mortality rates, while growth limitation and induced mortality by starvation do not seem to affect young shrimps (Henderson and Holmes 1989). However, in the 25-year data series study, predation did not have major impacts on C. crangon recruitments. An increase of predator abundance through time had no correspondence to abundance peaks on the C. crangon population (Campos 2009; Henderson et al. 2006). Therefore, cannibalism can be an important cause of juvenile mortality (Campos 2009). Moreover, in Swedish shallow waters it was estimated that 20% of the annual food consumption of C crangon might consisted of juvenile shrimps (Pihl and Rosenberg 1982).
C. crangon populations have a considerable degree of inter-annual variability, as was shown in long-term population studies, for example, 25 years in Bristol channel (Henderson et al. 2006), 30 years in the German Bight (Siegel et al. 2005) and 34 years in the Dutch Wadden Sea (Campos et al. 2010). In the Dutch Wadden Sea, environmental conditions from the previous winter, such as the amount of sunlight, salinity, fresh water discharge and the WNAOI, were correlated with autumn abundances. Spring abundances were correlated to the amount of sunlight and the NAOI in winter. In both seasons, abundances were positively correlated to annual commercial fishery (Campos et al. 2010). The population in the German
Bight showed another example of an inter-annual fluctuation. For autumn, on a large spatial scale, fluctuations in abundance were mostly correlated to year-to-year changes in biological and physical environmental parameters (winter water temperature, autumn river runoff and the WNAOI). On the other hand, on a regional scale, predation by gadoid was an additional component affecting the population size. Unlike the Dutch Wadden Sea, no correlations were found for such parameters for the C. crangon stock in spring (Siegel et al. 2005). In addition, C. crangon abundance peaks in Bristol Channel and Dutch Wadden Sea were positively correlated to the abundance of predators (Campos et al. 2010; Henderson et al. 2006).
Trophic interactions
The brown shrimp is considered a trophic generalist and a carnivorous opportunist, with a high rate of cannibalism (del Norte-Campos and Temming 1994; Lloyd and Yonge 1947; Marchand 1981; Pihl and Rosenberg 1984; Tiews 1970). Due to high abundances, it becomes an abundant prey, as well as a ubiquitous predator within its range (Gibson et al. 1995; Hiddink et al. 2002; Nehls and Tiedemann 1993; Norkko 1998; Oh et al. 2001). There-fore, it has been considered an important species within ecosystems, playing a key-role in trophic webs interactions (Pihl and Rosenberg 1984; van der Veer et al. 1998). C. crangon is simultaneously an important food resource for several species - like flatfish (Pleuronectes platessa), juveniles whiting (Merlangius merlangus), shore crabs (Carcinus maenas), seals (Phoca vitulina), various waders (Limicolae), gulls (Laridae), auks (Alcidae) and humans (Berghahn 1996; ICES 2011; Janke 1999 in Jung 2007; Jensen and Jensen 1985) - and an important predator on P. platessa (during and immediately after its settling stages) (Gibson et al. 1995; van der Veer and Bergman 1987), and on bivalves spat (e.g., Macoma balthica, Cerastoderma edule and Mya arenaria) (van der Veer et al. 1998), attaining important im-pacts on the latter. This species is also a significant predator on macrofauna communities, with a wide range of prey (e.g. 33 different types of prey were reported in United Kingdom estuaries) (Feller 2006; Nilsson et al. 2003). However, during food selection experiments, ju-veniles and adults showed weak meiofauna top-down impacts, despite harpacticoid copepods and other meiofauna taxa (mainly ostracods, foraminiferans and juvenile bivalves) decreased with the presence of C. crangon juveniles (Feller 2006; J¨onsson et al. 1993; Nilsson et al. 2003). In addition, in laboratory experiments, the juveniles’ impact on sediment microalgae and bacteria in sandy sediment is rather weak, showing no significant differences in oxygen fluxes, particulate organic carbon (POC) nor nitrogen (PON) content in the sediment. In the presence of juvenile shrimps, bioturbation of the microalgae mat appeared not to be signifi-cant, despite the changes of sediment characteristics due to their activity (J¨onsson et al. 1993).
9
Economic value
Brown shrimp is a common and highly appreciated food item in The Netherlands and Germany. In the North Sea this species is highly harvested, with 85% of the catch taken by Dutch and German fisheries. In 1997, the total value of landings was estimated to be about €98.2 million (Pascoe and Revill 2004). For the North Sea, about 27,000 ton / 75 billion individuals are caught annually, with an estimated total economic value on the fish market of €50-70 million (Revill and Holst 2004). Despite no great concerns have been assigned to this species’ status (Revill and Holst 2004), negative effects have been allocated on the population dynamics derived from by-catch discards or bottom trawling harm. Negative effects are also observed in food webs, related to indirect effects of shifts in shrimp abundances, induced by fishery (Berghahn and Purps 1998; Beukema and Dekker 2005; Blaber et al. 2000; Philippart et al. 2003; Vorberg 2000).
CHAPTER
3
Methodology
Sampling areas:
For comparison of the population characteristics near the latitudinal edges of Crangon crangon two estuaries were selected: the Minho River Estuary, situated in the northwestern coast of Portugal (41°N latitude, at Caminha), close to the southern edge of C. crangon range, and Valosen Estuary, situated in the north of Norway (67°N latitude, Bodø) at the northern limit of the species’ distribution (Figure 3.1).
Estuaries characterization
Minho Estuary, northwest of the Iberian Peninsula
The Minho River has an extension of about 300 km from its spring in Serra de Meira (Spain) to its mouth in the Atlantic Ocean with a northwest to southeast orientation. Com-prising a total basin area of 17,080 km2, with a mean annual freshwater discharge of 300 m3 s−1. The Minho Estuary has an extension of nearly 40 km, creating an estuarine area of 23 km2(Sousa et al. 2005). It has an averaged tidal range of 2.74 - 3.45 m (Instituto Hidrogr´afico 2010). Minho Estuary studies suggested it being a relatively undisturbed area, with low an-thropogenic pressure and contamination levels (Monteiro et al. 2007; Moreira et al. 2006; Quintaneiro et al. 2006; Reis et al. 2009). In terms of the biota characterization of Minho Estuary, only in the last decade several studies have been conducted to increase the knowledge about the principal faunal components present in the Estuary of River Minho. These studies focused on communities of macroinvertebrates (e.g. Sousa et al. 2007; Sousa et al. 2008a), epibenthos (e.g. Costa-Dias et al. 2010; Souza in prep, pers. comm.) and fishes (e.g. Antunes and Rodrigues 2004), some of them being conducted on invasive species (e.g. Sousa et al.
Figure 3.1: Location of the sampled estuaries, near the latitudinal edges of C. crangon species range: Valosen Estuary, (Norway) at the north edge and Minho Estuary, (Portugal) near the southern edge (adapted from Campos et al. 2009)
2008b; Sousa et al. 2008c). According to Sousa et al. (2008b) the subtidal macrozoobenthic fauna of the entire estuarine axis had a total of 68 taxa, including non-indeginous invasive species, e.g. Corbicula fluminea. The epibhentic community has been characterized, with five most abundant species in the lower Estuary: gobies (Pomatochistus minutus and Poma-tochistus microps), green crab (Carcinus maenas) and flat fishes (Platichthys flesus and Solea solea). Furthermore, the flounder (P. flesus), common goby (P. microps) and green crab (C. maenas), along with brown shrimp (C. crangon), dominated most of the lower Estuary, with high registered abundances of 14, 169, 62 and 500 ind 100 m−2, respectively (Costa-Dias et al. 2010). Minho Estuary also functions as a nursery ground for the brown shrimp and flat fishes (Costa-Dias et al. 2010).
Valosen Estuary, north of Norway
Valosen Estuary is located in the county of Bodø and comprises a small area that is totally exposed during low tide with a small river channel crossing the tidal flat. The river mouth is located inside a large bay in the northwest of Norway. The estuary has an east to west orientation and has a tidal range of 2 - 2.4 m (Freitas et al. 2010). There is no study for the anthropogenic impacts for this estuary. The local direct anthropogenic impacts can be infer to be low, due to the low human abundances in the surrounding area of the estuary, 34 persons km−2 during the years 2005 and 2006 (Statistics Norway, 2011). However, a study for the Norway coastal waters shown unusual high levels of inorganic arsenic (Sloth and Julshamn 2008).
13
With only two previous studies, the Valosen Estuary is not a very well known ecosystem. One of these studies, focused on the habitat quality as a subartic nursery for plaice (Pleuronectes platessa) during the years 2005 and 2006 (Freitas et al. 2010). In this study the epibenthic and benthic communities were characterized; in 2005, the macrozoobenthos assemblages 10 taxa were identified, with bivalves (Cerastoderma edule and Macoma balthica) being the most abundant. For both years, the epibhentic community was constituted by green crabs (C. maenas), brown shrimp (C. crangon), sand goby (P. minutus) and flatfishes (P. flesus and P. platessa). With the density peaks registered for green crab of 25 ind 100 m−2, and for the fish community, the plaice (P. platessa) was reported to be 65 ind 100 m−2, sand goby with 16 ind 100 m−2 and flounder 6 ind 100 m−2. The brown shrimp was the most abundant species with density peaks of 250 ind 100 m−2(Freitas et al. 2010).
Sampling strategy:
The C. crangon population in the Minho Lower Estuary was monthly sampled from April 2009 to July 2010, on spring tides during the high tide, at three sampling stations (Figure 3.2), with three replicates per site. In the Valosen Estuary, sampling was performed every two weeks during 2005 and 2006, from April to October, on neap tides during the high tide, at three sampling locations (Figure 3.3) with two replicates per site. In Norway, sampling during the winter was impossible due to ice cover.
In both estuaries, was used with a 1 m wide beam trawl, 5 mm mesh-size at the cod end. Each tow lasted 3 minutes at a constant velocity of 2 km h−1, which sampled an area about 100 m2. At each site in Minho Estuary, environmental variables (temperature (°C), salinity, pH, and redox potential (mV)), were registered in situ near the bottom, with two replicates per site, using a multiparametrical sea gauge YSI 820. Valosen Estuary temperatures (°C) and salinity values were registered continuously with a logger moored at the bottom (Stow-Away®TidbiT™). Temperatures were determined for high tide only and averaged for every week. Temperature logger did not record temperatures in 2006 from mid-July to beginning of August. Therefore temperatures were estimated from a nearby station at Skrova. The Skrova station is located at 68°07’ N, 14°39’ E and had a good correlation among the tem-peratures registered in 2005 with Valosen Estuary during the sampling period. This relation was already shown by Freitas et al. (2010).
Sample analysis:
C. crangon total length (TL) was determined as the distance between the end of folded uropods/telson and the tip of scaphocerites. Sex and maturation stage were determined by the differences in size and shape of the endopodite of the first pleopod and the presence or absence of the masculine appendix on the endopodite of the second pleopod. Thus, specimens were classified as mature males, mature females, bearing females and indeterminate. Sex was
Figure 3.2: Map showing the location of the sampling stations in the Minho Estuary, Portugal determined whenever possible, even for specimens under 15 mm. Density of bearing females was estimated and sexual maturity was set for females by the presence of attached eggs. Individual biomass was determined for a representative number of individuals of different lengths for females and males at both estuaries. In Minho Estuary, individual biomass was determined from May 2009 to July 2010 and in Valosen Estuary this was done from April to October 2006. The biomass was determined in ash free dry mass (AFDM), calculated as the difference between dry (48 h; 60°C) and ash weight (4 h; 420°C).
Data analyses:
To characterize the sampling sites at the Minho Estuary, a Principal Components Analyses (PCA), with the environmental variables measured at each station, was performed with the Primer 6 software (Clarke and Gorley 2006). Furthermore, comparisons within abiotic factors on spatial and temporal scales were performed by the nonparametric Kruskal-Wallis test, using MINITAB14 (Arend 1993).
Distribution and abundance patterns were assessed based on monthly distributions. Ju-venile densities were determined by individuals with a total length lower than 15 mm, from both sex classes. Abundance data was expressed in densities as individuals per 100 m2 and averaged by sampling area. In order to test if temporal and spatial scales had any influence on C. crangon distribution, a one-way ANOVA analyses was performed, followed by the Tukey post-hoc test whenever significant results were found. These statistical analyses were done using MINITAB14 (Arend 1993). A Canonical Correspondence Analyses (CCA) was used to evaluate population temporal and spatial distribution correlated to abiotic factors, using XLSTAT - Microsoft Excel.
Sex-ratio was determined for mature individuals in each month, as total number of males per females. The sex-ratio variation was plotted against juvenile densities and reproductive
15
Figure 3.3: Map showing the location of the sampling stations in the Valosen Estuary, Norway (adapted from Freitas et al. 2011)
events were identified.
The relationship between AFDM and TL
AF DM = a ∗ T Lb (3.1)
was linearized by applying logarithms to both sides of the equation resulting in:
log(AF DM ) = log(a) + b log(T L) (3.2)
Changes in this relationship between months were compared for males and females, within each estuary. For the Minho Estuary the comparison covered one year period (August 2009 to July 2010) while, for the Valosen Estuary, only seven months of 2006 were used (April to October). These linearized regression lines within each sex class were tested for coincidence between lines, and if they were not coincident then they were tested for differences between slopes. Whenever significant differences between slopes were identified, a Tukey post-hoc test was used to compare them.
Cohorts were established using ANAMOD software, based on size-frequency distribution for 2 mm length classes, on consecutive sampling events. The best fit between expected and observed age class distributions was assessed with the G test (Nogueira 1992).
All statistical tests used a statistical significance of 0.05.
Production was estimated based on cohort recognition. Production increments (P) and elimination production (E) were calculated with a method derived from Allen (1971), as described by Dauvin (1986). Approximated values of P and E for each cohort during a time
interval were expressed as: P = Nt+ Nt+1 2 Wt+1− Wt (3.3) for Wt+1 > Wt E = Wt− Wt+1 2 (Nt+ Nt+1) (3.4) for Nt > Nt+1
N: density of the cohort in each sample date; W: mean individual biomass in each sample date; t and t+1: consecutive sample dates.
Total values for P and E for each cohort were expressed as:
P = t=0 X t=n (Nt+ Nt+1) 2 ∆W (3.5) E = t=0 X t=n (Wt+ Wt+1) 2 ∆N (3.6)
For total values of P and E for the population were expressed as:
P = N X n=1 Pcn (3.7) E = N X n=1 Ecn (3.8)
for (Pcn) growth and (Ecn) elimination production of the cohort n.
Ratios of P /B and E/B were determined. Being B calculated as:
B = 1 T N X n=1 Bnt (3.9) T: period of study; N= number of successive cohorts in the period of T; Bn was the biomass of the cohort n; t: for the duration of the cohort n.
CHAPTER
4
Results
4.1
Minho Estuary, northwest of the Iberian Peninsula
Abiotic factors
The Principal Components Analyses (PCA) for the abiotic data, measured from May 2009 to April 2010, show clear differences for station 1 compared to stations 2 and 3 (Figure 4.1). Station 1 (closest to the river mouth), was characterized by higher depth and salinity values. Station 2 was located within a salt marsh, with large variations in salinity and depth values during the sampling period. In station 3, the upstream station, high salinity values were only reported for a short period in summer and early autumn.
Stations had no significant differences in temperature and pH values (H = 1.28; p= 0.528 and H = 2.23; p= 0.328). However, these factors were highly significantly different among seasons (H= 18.76; p= 0.000 and H = 18.48; p= 0.000) as temperatures were lower in winter and early spring and pH values were lower for winter and spring months. Salinity and depth varied significantly among stations (H = 20.62; p= 0.000 and H = 28.85; p= 0.000), with no significant variation on a temporal scale (H = 5.53; p= 0.137 and H = 6.55; p= 0.088). For redox potencial (ORP) values no statistical significant differences were determined among seasons nor stations (H = 4.47; p= 0.215 and H = 0.13; P= 0.936). The abiotic factors measured at the sampling sites and the statistical analyses are shown in Appendix A and B, respectively.
Figure 4.1: Principal Components Analyses (PCA) showing the differences of the environ-mental variables among sampling stations at the lower estuary, for the period of May 2009 to April 2010; s = station 1; l = station 2 and n = station 3. Factors: T(°C) = water temperature; ORP(mV) = potential redox; pH; Salinity and Depth (Data provide by Allan Souza, 2011)
Population structure
Spatial and temporal distribution
For population analyses a total of 8,942 individuals were examined, 2,530 males, 6,215 females (from which only 73 were bearing females) and 139 with indeterminate sex. For 58 individuals, representing 1.23% of captured population, it was not possible to determine sex. The average density for all stations combined, within the full sample period, was estimated to be 572 ind 100 m−2.
Within the estuary, the population had significant seasonal fluctuations during the sam-pling period (F=6.38; p=0.000). The highest densities were registered in summer, in June and July ( 945 and 1011 ind 100m−2), and in the summer/autumn transition (September 2009) reaching 1,404 ind 100 m−2. This peak was followed by a drop in November, after which the population increased slowly, with a small winter peak in December (871 ind 100 m−2).
4.1 Minho Estuary, northwest of the Iberian Peninsula 19
The lowest values were registered in early spring (April) in both years (with 80 and 110 ind 100 m−2, for 2009 and 2010 respectively) (Figure 4.2(a)). After the lower values registered in spring, it was noticeable a increasing pattern in both situations. A Tukey post-hoc test showed that summer had significantly higher density values compared to winter and spring. One-way ANOVA and post-hoc test results can be consulted, respectively, in Appendix C and D.
Crangon crangon densities varied significantly among the sampling stations (F= 13.86; p= 0.000). Station 1 had higher densities in winter and early spring (from November to April), with an evident decrease in densities from August to November. This period coincided with the highest density values recorded at station 3. At station 2 high densities values were registered for most of the sampling period. In this station the lowest values were recorded in two consecutive months in early spring (April and May 2009; March and April 2010) (Figure 4.2(b)).
Distribution data were analyzed for the life stages and genders: mature individuals (fe-males and (fe-males), bearing fe(fe-males and juveniles. Fe(fe-males showed the most significant differ-ences among seasons (F= 8.26; p=0.000) and stations (F= 10.27; p= 0.000). The post-hoc results for spatial density distribution of females showed that station 2 was significantly dif-ferent from the others because of its higher density values. On a temporal scale, summer and spring were significantly different from the other seasons, with the highest and lowest average densities values, respectively. Male density variations showed a clear difference in spatial distribution (F= 16.41; p= 0.000), with the lowest density values at station 3, being significantly different from the others in the post-hoc test. No significant differences in male densities were registered among seasons (F= 0.55; p= 0.652). However, in winter it can be observe an increase of densities in station 1.
Bearing females were not analyzed for spatial or temporal distribution with ANOVA analyses, due to the relatively low percentage of the total captured females (1.17% of total). These individuals were only captured at the lower part of the estuary (station 1), in the summer and spring months (Figure 4.2(e)). The peaks of juveniles densities were observed between June and August of 2009 (average of 160 individuals 100 m−2) and in May 2010 (256 individuals 100 m−2). Juvenile recruitment had significant seasonal and spatial density variations (F= 4.20; p= 0.007 and F= 10.22; p= 0.000), with significantly higher densities in spring, mainly in station 2 (Tukey post-hoc test). Juveniles were only reported at the upstream station in July and August, 2009 (Figure 4.2(f)). One-way ANOVA and post-hoc test results can be consulted, respectively, in Appendix C and D.
Salinity and temperature driven migratory behaviour was observed at station 1: when the system was under low values of temperature and salinity, shrimps moved towards the mouth of the river, reaching for higher salinities. Upstream migratory movement, observed at station 3, seemed to be more related to salinity rather than temperature, as high densities values were
(a) Estuary (b) Sampling stations
(c) Mature females (d) Mature males
(e) Bearing females (f) Juveniles
Figure 4.2: Crangon crangon density variations during the sampling period, from April 2009 to July 2010, (a) for the estuary, (b) for each sampling station and for the different groups: (c) females and (d) males, (e) bearing females, (f) juveniles
only recorded with high salinity values. No pattern on migratory behaviour could be observed in station 2. In this area the presence of C. crangon was more related to recruitment and overall population density peaks than to environmental variables.
The Canonical Correspondence Analyses (CCA) for spatial and temporal distribution, us-ing abiotic factors and individual classes as variables, demonstrated the inexistence of a linear relationship between those variables (p= 0.554). From the total variance, 69% was explained
4.1 Minho Estuary, northwest of the Iberian Peninsula 21
by abundance patterns and 23% by the environmental - species abundance relation. However, the CCA analyses showed that mature male distribution was influenced by salinity values. Mature female distribution did not seem to be strongly influenced by the environmental vari-ables, however, bearing females showed a preference for deep water. Juveniles favoured the salt marsh location (station 2) during spring, on their highest density point (Figure 4.4).
Sex-ratio
The sex-ratio among mature individuals always favoured females (Figure 4.5). Never-theless, males had higher densities in April and June 2009, and in May 2010, with a small increase of male density in winter months (October to December 2009). The high values for male density were followed by an increase of juvenile density. Therefore, these periods of high male density were assumed to be, simultaneously, occasions when reproductive events occurred with higher frequency.
Population dynamics
The smallest individual, measuring 6.5 mm, was captured in October 2009 and the biggest, a 58 mm bearing female captured in April 2009. Males had a maximum total length of 43.5 mm. Indeterminate individuals were found among all size classes, from 6.5 to 35 mm. Bearing female size range from 26.5 found in July to 56 - 58 mm in April months. Due to the low abundance of bearing females throughout the sampling period, no correlation could be found in the frequency of reproduction events, fertility values, nor larvae survival to the juvenile stage. Juveniles represented 12.64% of the total catches, therefore, this estuary is an important nursery ground for this species, and their presence throughout all the sampling period suggests continuous reproduction.
Size distribution was determined for all stations combined and for each station separately, for the overall population and sex classes (males and females) (Figure 4.6). In the overall population the mean size of 22 mm had the highest frequency of occurrence, with 30% of the total catches. Sizes over 22 mm, individuals become less frequent for the overall population.
Table 4.1: Mean values and standard deviation for densities (ind 100 m−2) per station during the sampling period from April 2009 to July 2010, for mature males (M), mature females (F), bearing females (BF), juveniles (J) and total abundance (T); with the first number being the mean and the second the standard deviation
Stations M F BF J T
St1 169.31 (±181.998) 204.08 (±222.664) 5.33 (±16.711) 51.60 (±88.916) 385.90 (±404.032)
St2 211.64 (±200.531) 760.72 (±623.932) 0.00 (-) 140.44 (±190.001) 986.76 (±775.310)
Temperature Salinity
(a) Station 1
(b) Station 2
(c) Station 3
Figure 4.3: Spatial and temporal variations on Crangon crangon densities, according to sex class (juveniles, matures males and females) for the abiotic factors, temperature and salinity measured at each sampling event
Smaller individuals sizes were more frequent for station 2. (Figure 4.6(a)). Females were most abundant in the 20 mm class and reached higher size values, although males were more abundant in the 27 mm class (Figure 4.6(b), (c)).
The total length-biomass relation was determined for a total of 1,704 individuals. The length-biomass equation was determined for the total population for each month from May 2009 to July 2010 (Appendix E - Table E.1). For one year period, from August 2009 to July 2010, linear regression were determined for the overall population and the sex classes (female and male) (Figure 4.7(a), (b), (c)). Individual trend lines for males and females were
4.1 Minho Estuary, northwest of the Iberian Peninsula 23
Figure 4.4: Canonical Correspondence Analyses (CCA) analysis for Crangon crangon popu-lation densities from April 2009 to July 2010 (Sex classes: M, mature males ≥15 mm TL; F, mature females ≥15 mm TL; Fo - Bearing females; J, juveniles < 15 mm TL; Abiotic factors: Sal, Salinity; T, Temperature; Dpt, depth; ORP, redox potential; pH; Seasons: Sp, spring; Su, summer; At, autumn; Wt, winter; and Stations: 1, 2, 3)
determined at each month for the same period of one year (Appendix E - Figure E.2). In the ANCOVA analyses for males and females, the linear regression lines were not coincident, with significant differences among slopes and elevation point values (Table 4.2 and Figures 4.7(e), (d)). Differences between slopes calculated for each month regarding females and males were determined by the Tukey post-hoc test (see Appendix E - Table E.3).
For females models with the highest slope values were determined from February to June and August, and these months showed no significant differences among them. The lower slope values from September to January were significantly different from April to June. July had the lowest value and was significantly different from all the other months (with the exception of November and January). From these results we could infer that lower body mass increments occur during winter months, due to the investment required to survive harsh environmental conditions and reproduction investment. The higher values observed for summer months could be a consequence of more favourable environmental conditions, despite that in this
Figure 4.5: Sex-ratio and juveniles total abundance of Crangon crangon during the sampling period; bars show the density of juveniles for all stations combined and black line the variation on sex ratio, as the total males individuals divided by females
(a) Total captured individuals (b) Total of captured females (c) Total of captured males
Figure 4.6: Size structure from catches of Crangon crangon at each station (1, 2, 3) during the sampling period, for the total catches of (a) total individuals, (b) females and (c) males; the size classes are indicated with the mean value for each class interval
period the investment for reproduction seems to be higher. However, the lowest value in July was not correlated to the remaining summer months and it cannot be explained by this data. For males, higher slope values were recorded from spring (March) to autumn (October), with the exception of a lower value in July. The lowest slope values were determined for winter months, from November to February. Male biomass increment pattern seems to be related to prevalent seasonal conditions.
4.1 Minho Estuary, northwest of the Iberian Peninsula 25
(a) Overall trend line for all individuals
(b) Overall trend line for all females (c) Overall trend line for males
(d) Individual trend lines for females (e) Individual trend lines for males
Figure 4.7: Total length biomass relation of Crangon crangon during the one year sampling period, (a) for total individuals; (b) females and (c) males, and individuals regressions lines for each month (d) for females and (e) for males
integrated all the individuals captured. Multiple generations co-exist in this ecosystem, from 5 to 8 generations (Figure 4.8). The mean growth of individuals for all cohorts was estimated to be 0.12 mm d−1± 0.067 (mean, standard deviation). It is noticeable a growth rate decrease in mature individuals from November to March. According to these data, the average life span of C. crangon on this estuary was estimated to be 0.73 years.
Figure 4.8: C. crangon modal class analysis during the sampling period, from April 2009 to July 2010
Production estimation
To calculate the annual production, length - biomass relation was determined for each month for all individuals (Appendix E - Table E.1).
The growth production was estimated to be 264.18 mg AFDM m−2 y−1 and the elimina-tion producelimina-tion 366.89 mg AFDM m−2 y−1. The cohort interval was 195 days on average. The production/biomass ratio was 6.38 and the elimination/biomass ratio was 8.86. Calcula-tion for producCalcula-tion and eliminaCalcula-tion producCalcula-tion for each cohort can be consulted in Appendix F, for the annual production see Appendix G.
Table 4.2: ANCOVA results for total length - biomass relationship on the linear regression lines, for males and females
Males Females
Coincidental regressions F= 236.35 p= 0.000 F= 184.39 p= 0.000 Slopes comparison F= 423.06 p= 0.000 F= 289.96 p= 0.000
4.2 Valosen Estuary, north of Norway 27
4.2
Valosen Estuary, north of Norway
Abiotic factors
In both years, temperatures were lower in early spring and then gradually increased until summer, with peaks in June 2005 and August 2006. After theses peaks, values of temperature decreased till October (the last month sampled). Temperature values did not significantly differ among the years (Campos et al. 2009). Due to discontinued recording (technical problems with the data logger), it was not possible to determinate salinity values at each sampling event. However, the data recorded during two months (April and May), showed that low tide salinity had values of 0 and high tide salinity was always around 30 (close to marine salinity) (Appendix H). This data is in line with the total exposure of the estuarine area during low tide. Also, due to a low freshwater input , marine waters seem to be the major contribution for the water column during high tides.
Figure 4.9: Temperatures (°C) measured in Valosen Estuary, with the estimated temperatures from Skrova station represented with a dashed line (adapted from Freitas et al. 2011)
Population structure
Spatial and temporal distribution
From the 2005 sampling, a total of 8,124 common brown shrimp individuals were exam-ined; 4,605 males, 3,423 females, from which 140 were bearing females, and 94 indeterminate individuals. For the sampling period of 2006, a total of 9,168 individuals were examined, with 3,972 males, 4,882 females, from which 216 were bearing females, and 314 indeterminate shrimps.
The Crangon crangon population showed different density patterns within the two sam-pling periods (Figure 4.10(a)). In 2005 the overall population density showed abrupt changes. Population peaks in April (104 ind 100 m−2) and July (137 ind 100 m−2) were followed by low density values in June (40 ind 100 m−2) and August (71 ind 100 m−2). After August, density values started to increase, until reaching a maximum value in October (138.5 ind 100 m−2). In the year 2006, the population had a density increasing from the lowest values, recorded from April to June (around 30 ind 100 m−2), to its peak in September (269 ind 100 m−2).
The overall population density within the sampling periods was averaged to be 97 and 124 ind 100 m−2), for 2005 and 2006, respectively. Between both years densities showed no significant differences for the overall population (F= 2.70; p= 0.102), as well as for mature males (F= 0.33; p= 0.564), bearing females (F= 3.23; p=0.074) and juveniles (F= 0.34; p= 0.559). The mature female density (non bearing females and bearing females) was significantly different (F= 8.22; p= 0.005) between the two years, with a significant difference (F= 7.38; p= 0.007) for the non bearing female density (Appendix I - Table I.1).
In both years the overall population density pattern reflected the densities registered at each sampling stations (Figure 4.10(b)). However, in 2005 station 1 was an exception from June to August, with considerably lower density values in the population density peak. During this year station 3 had higher densities for most of the sampling period. In 2006, the density pattern was similar in all stations, with lower values for station 1. For each year, significant differences in densities were determined for each sex group among sampling stations and months. In 2005, spatial distribution showed no significant variations for the total population (F= 0.94; p= 0.393), as well as, for mature males (F= 0.89; p= 0.415), mature females (F= 2.54; p= 0.085) and juveniles (F= 2.70; p= 0.073). Only bearing females showed significant differences (F= 6.71; p= 0.002), with post-hoc test results returning significant differences between station 1 and 3. On a temporal scale, significant differences were observed for bearing females and juveniles (F= 5.60; p= 0.000 and F= 3.34; p= 0.006, respectively), with July being significantly different for both bearing females and juveniles. ANOVA and post-hoc test results can be found in Appendix I - Table I.2 and Appendix J - Table J.1.
In 2006, stations showed significant differences on spatial distribution for mature females (F= 4.97; p= 0.009), bearing females (F= 6.89; p= 0.002) and juveniles (F= 3.71; p= 0.029). Significant differences were determined for mature males between station 1 and 3. For bearing females and juveniles, stations 1 and 2 were significantly different. On temporal density variations, ANOVA results were most significant for every group: mature males (F= 23.57; p= 0.000), mature females (F= 12.58; p= 0.000), bearing females (F= 9.34; p= 0.000) and juveniles (F= 5.67; p= 0.000 ). In the post hoc test, for the mature males, mature females and bearing females, we could identified a group from August to October that was significantly different from the other months. In the case of bearing females differences were for lower density values. In juveniles significant differences were present for July and August when
4.2 Valosen Estuary, north of Norway 29
(a) Estuary (b) Sampled stations
(c) Mature females (d) Mature males
(e) Bearing females (f) Juveniles
Figure 4.10: Crangon crangon densities during the sampling period from April to October in 2005 and 2006 for (a) the estuary, (b) for each sampling stations, and for the different groups: (c) mature females, (d) mature males, (e) bearing females and (f) juveniles
compared to all the other months. ANOVA and post-hoc test results can be consulted in Appendix I - Table I.3 and Appendix J - Table J.2.
In both years, a continuous reproduction can be suggested by the capture of bearing females throughout the sampling period at all stations. This situation can be reinforced by presence of juveniles in the same period.
Bearing females represented 4.08% and 4.42% of the total captured females, for 2005 and 2006, respectively. The total size distribution in the sampling period appears to be random, with small and larger sizes in all months in both years (Figure 4.11). According to the density
Figure 4.11: Box-plot for Crangon crangon bearing females size distribution during the sam-pled period, April to October in 2005 and 2006
values, bearing females showed a preference for the station closer to marine waters (station 1), with a decreasing density along the estuary axis for the majority of the sampling months. A relatively higher value for this group was observed at station 1 on April 2005 (7 ind 100 m−2). This first peak for bearing females, infers an earlier reproduction event, when compared to the following year. In this same year, a second peak for July was observed with a averaged density of 5 ind 100 m−2 for the estuary. On the second year, bearing female densities had a high value from May to July (averaged in 4 ind 100 m−2).
The total juveniles captured represent 1.49% and 1.55% of total catches for 2005 and 2006 sampling campaigns, respectively. Juvenile high density peaks were noticeable in July 2005 and August 2006, with combined density values for all the stations of 5.25 and 6.67 ind 100 m−2, respectively. In the first year juveniles were more abundant in the upstream station and in the second year higher density values were reported for station 2.
Sex-ratio
Sex-ratio was determined for both years. In the first year the sex-ratio favoured males and the relation between sex-ratio values and juvenile recruitment should be analyzed when values were lower (i.e., when female density increased). The even ratio in May is possibly related to the juvenile density peak in June and the higher value in August . However, in the second year, sex-ratio values favoured females. Therefore, when the sex-ratio value increased by the higher presence of males, this was followed by higher densities of juveniles. The high value in June was probably related to the high densities in juveniles in July and/or August and the sex-ratio in September has probably produced the winter brood.
4.2 Valosen Estuary, north of Norway 31
Figure 4.12: Sex ratio and juveniles density of Crangon crangon during the sampled period; bars show the density of juveniles for all stations combined and black line the variation on sex ratio
Population dynamics
For the overall sampling period, the smallest C. crangon was captured in May 2005 with 9 mm and the largest individual captured (October 2005) was a female measuring 70 mm. In this estuary bearing female size class ranged from 37 to 65 mm. The biggest male was 57 mm (August 2006). Indeterminate individuals were found in all size classes ranging from 11 to 54 mm.
Size distribution was determined for the totality of captured individuals, males and fe-males, all stations combined and within stations, and for each year separately (Figure 4.13). In 2005, total captures showed two peaks in the size distribution at 22 and 37 mm, with the highest abundance (18%) for the former. After the second peak, the total number of individuals witin the highest size classes started to decrease till the highest value reported (70
Table 4.3: Mean values and standard deviation for densities (ind 100 m−2) per station during the sampling period from April to October in 2005 and 2006 for mature males (M), mature females (F), bearing females (BF), juveniles (J) and total abundance (T); with the first value being the mean and the second the standard deviation
Year Station M F BF J T 2005 St 1 58.11 (±63.022) 30.92 (±32.636) 3.11 (±3.583) 0.50 (±1.036) 90.86 (±94.024) St 2 42.11 (±34.77) 39.43(±36.395) 1.57 (±3.108) 1.07 (±2.418) 83.86 (±72.260) St 3 59.39 (±59.934) 49.27 (±37.731) 0.32 (±1.362) 2.75 (±5.973) 115.36 (±101.330) 2006 St 1 43.70 (±52.652) 35.37 (±31.784) 4.15 (±4.026) 0.48 (±1.156) 88.93(±91.124) St 2 47.929 (±56.607) 68.11 (±61.600) 2.43 (±2.795) 3.29 (±6.005) 132.18 (±127.919) St 3 53.23 (±55.910) 81.97(±73.795) 1.11 (±2.006) 1.57 (±2.588) 149.20 (±136.050)
