Defence on Demand : A physiological perspective on phenotypic plasticity in anti-predator traits

Almost all species face some degree of predation risk, and, hence, evolution has produced a plethora of anti-predator defences. However, anti-predator strategies require resources, and the prevailing risk of becoming prey is influenced by many factors and rarely constant across time and space. Evolution has therefore favoured the development of phenotypic plasticity in anti-predator defences. The capacity of a single genotype to fine-tune its phenotype according to the prevailing risk of predation results in a closer phenotype-environment match in the mercurial environments of the natural world. Interest in the ecology and evolution of inducible defences has progressed the development of its theoretical underpinnings, along with empirical tests of theoretical predictions. Inter-individual differences in the expression of inducible traits are nowadays understood ubiquitous, and this intriguing variation holds possibility to bridge our current knowledge gap on the proximate, physiological mechanisms underlying inducible morphological defence regulation. In this thesis, I address unanswered questions on the proximate, physiological processes behind phenotypic plasticity in morphological defences. I first examine classic resource-allocation trade-offs to search for hidden physiological costs coupled with perceived predation risk and investment into a morphological defence. I further employ a recent hypothesis of physiological stress being the mechanism driving morphological defence regulation. To test my predictions, I have used a well-established model system for the study of inducible morphological defences, the crucian carp (Carassius carassius). I show that innate immune functions are altered by predator exposure, and that the defence against pathogens is correlated with the morphological defence against larger-sized enemies (predators). Second, from a series of laboratory experiments and field studies, I demonstrate support for the hypothesis of stress physiology being involved in plastic defence expression, and that crucian carp display clear sexual dimorphism in the anti-predator phenotype. I suggest that this is due to sex-specific trade-off dynamics, where females invest more into reproduction, resulting in less resources for anti-predator protection. Finally, I present novel trait changes (changes in body colour, diel activity and eye morphology) in response to non-lethal predation risk that may act in synergy to produce an integrated anti-predator phenotype. In summary, my results illustrate a potential causality from the vertebrate stress axis to the regulation of morphological defence expression. Further, my thesis highlights variation and complexity on the route to producing optimal anti-predator phenotypes under competing demands from other interests

Developing management goals and associated assessment methods for Sweden’s nationally managed fish stocks : a project synthesis

This report summarizes and synthesizes results from the Swedish Agency of Marine and Water Management (SwAM, or HaV) funded project “Förvaltningsmål för nationella arter (Management goals for nationally managed species)”. The objectives of the project have been to promote the development of management goals and associated status assessment methods and indicators, as well as reference points, for some nationally managed fish stocks both in coastal as well as freshwater areas. The report focusses largely on species and stocks that can be defined as data-poor. Such stocks are characterised by marked limitations in data availability and/or resources allocated to detailed analytical stock projections. Data-poor stocks also often lack carefully formulated management goals and associated methods and indicators for assessing stock status. In this report, we provide an overview of potential assessment methods and indicators and try to synthesise how they work and what the strengths and weaknesses are by applying them to selected data poor stocks such as pikeperch, pike, whitefish, and vendace. We also discuss how they relate to different potential management goals and provide recommendations for their application. We grouped the indicators and assessment methods by the three categories that are now used in the yearly status assessment framework provided by SLU Aqua (Resursöversikten/Fiskbarometern) – i) mortality, ii) abundance/biomass and iii) size/age structure. The results are also described for these three main categories of assessment indicators. Included is also a status report from a size- and age-based population dynamics model (Stock Synthesis 3) that is being developed for pikeperch in Lake Hjälmaren.An important experience from the project is that to improve the assessment methods for Swedish national fish stocks, it is important that managers develop both general as well as more detailed quantitative goals for the individual stocks. This should ideally be conducted in various forms of collaboration with the main stakeholders and scientists involved with assessment as participatory processes foster legitimacy. Carefully articulated management goals, which are possible to translate into quantitative targets, will facilitate the development of various approaches and methods to monitor stock statuses. Given the strong and complex interactions of fish and their environments it is also important to consider other pressures than fisheries when developing indicators and assessment methods.Our synthesis highlights a number of areas where the assessment of data-poor stocks can be improved:1. Apply precautionary principles for data-limited stocks, particularly ones that are known to be vulnerable to exploitation.2. Tailor approaches to how fisheries are managed in Sweden. Swedish nationally managed fish stocks are not managed by quotas (with one exception, vendace in the Bothnian Bay) and do not aim for maximum sustainable yield. Instead, the coastal and inland fisheries are managed by regulating the effort in the small-scale commercial fisheries (number of fishers/licenses and amount of gear). Regulation of recreational and subsistence fisheries effort, in terms of licenses or number of fishers) is not applied, nor possible since the fisheries is lacking obligatory notification and reporting systems. All national fisheries, however, are regulated by various technical measures (closed areas, size-limits, bag-limits, gear restrictions etc). Thus, goals and assessment methods that result in harvest limits or quota recommendations expressed in e.g. biomass/numbers are difficult to use as basis for management. Instead, there is a need for alternative management goals and associated assessment methods.3. Use best practice methods and indicators and adapt as scientific knowledge is developed. Data-limited methods are developing rapidly, and new methods/approaches are proposed in the scientific literature every year. It is thus important to be updated on the most recent developments. 4. Clearly describe limitations/assumptions of methods used. It is important to be aware of and critically evaluate the assumptions underlying the analyses, and to carefully communicate uncertainty together with the stock status assessment.5. Be particularly careful with low sample numbers. Many indicators and methods can be applied also on small sample sizes, however, the accuracy and precision of the estimates risk being low in such cases.6. Accept that there is no "gold standard" for fisheries assessment. Each case study is unique and needs to be balanced against data availability, local needs and other important factors. This also means that analysts need to be careful when using generic reference levels or “borrowing” data from other stocks.7. If possible, use several different methods/indicators. Although several indicators aim to measure similar aspects of the stock, small methodological differences can support the overall interpretation of individual indicator values. It is particularly important to incorporate many aspects and indicators (size/age/abundance/mortality) in order to produce a balanced assessment.8. Develop means of communication. Indicators and goals should be easy to understand. However, interpretation of results from multi-indicator frameworks can be challenging. There is thus a need for finding ways of communication that can convey complicated results in a simple-to-understand manner.9. For details on additional improvements, we refer the reader to the sub-header “recommendations for the future” found under each chapter.The implementation of Stock Synthesis for pikeperch in Lake Hjälmaren showed that it is possible to develop a more ambitious and detailed stock assessment model for a relatively data-poor stock. The model results partly support earlier interpretations of the development of the stock and the importance of the changes in regulations in 2001 (increased minimum size, increased mesh size and reduced mortality of undersized pikeperch). Before the model can be implemented and used for practical management, a number of actions for improvement are needed, which are highlighted in the relevant chapter. The most important next step is establishing management goals and reference levels for this stock. We recommend that such a dialogue is initiated by managers. The fisheries management goals should consider both biomass, fisheries mortality and size-based targets.To conclude, we stress the importance of improving all ongoing aspects related to the assessments of data-poor Swedish stocks. Strong local stocks and sustainable fisheries are vital for a variety of fisheries-related businesses and practices, particularly in rural areas, providing economical and societal value. Fishes also have important roles in aquatic food-webs and it is important that ecological values are managed wisely in order to reach targets for water quality, ecosystem structure and diversity. Given the strong and complex interactions of fish and their environments it is also important to consider other pressures than fisheries when developing indicators and assessment methods

Predation risk and the evolution of a vertebrate stress response: Parallel evolution of stress reactivity and sexual dimorphism

Predation risk is often invoked to explain variation in stress responses. Yet, the answers to several key questions remain elusive, including the following: (1) how predation risk influences the evolution of stress phenotypes, (2) the relative importance of environmental versus genetic factors in stress reactivity and (3) sexual dimorphism in stress physiology. To address these questions, we explored variation in stress reactivity (ventilation frequency) in a post-Pleistocene radiation of live-bearing fish, where Bahamas mosquitofish (Gambusia hubbsi) inhabit isolated blue holes that differ in predation risk. Individuals of populations coexisting with predators exhibited similar, relatively low stress reactivity as compared to low-predation populations. We suggest that this dampened stress reactivity has evolved to reduce energy expenditure in environments with frequent and intense stressors, such as piscivorous fish. Importantly, the magnitude of stress responses exhibited by fish from high-predation sites in the wild changed very little after two generations of laboratory rearing in the absence of predators. By comparison, low-predation populations exhibited greater among-population variation and larger changes subsequent to laboratory rearing. These low-predation populations appear to have evolved more dampened stress responses in blue holes with lower food availability. Moreover, females showed a lower ventilation frequency, and this sexual dimorphism was stronger in high-predation populations. This may reflect a greater premium placed on energy efficiency in live-bearing females, especially under high-predation risk where females show higher fecundities. Altogether, by demonstrating parallel adaptive divergence in stress reactivity, we highlight how energetic trade-offs may mould the evolution of the vertebrate stress response under varying predation risk and resource availability

Åtgärdsprogram för mal : (Siluris glanis)

Åtgärdsprogrammet syftar till att förbättra malens (Siluris glanis) överlevnad i landet. Det är ett vägledande, men ej legalt bindande, aktionsprogram.  Malen är Sveriges största sötvattensfisk. Den största mal som fångats i Sverige var 3,6 meter lång och vägde uppskattningsvis 180 kg. Malen vandrade in till Sverige under Ancylus-perioden, när Östersjön var ett varmt och sött innanhav.  Malen lever i sjöar och flodmiljöer. Den är allätare och kan utöver fisk även äta groddjur, gnagare, fåglar, kräftor, insekter, maskar och blötdjur. Malen är revirhävdande, framför allt under lektiden. För sin reproduktion är den beroende av varmt vatten samt vattenväxter och strandnära vegetation. Hanen bygger ett bo bland vegetation och rötter dit honan lockas för lek. Hanen vaktar sedan äggen tills de kläckts. Ungarna växer upp i skydd av vegetationen.    I Sverige var arten mer spridd förr, men förändringar i markanvändningen från 1800-talets mitt, med exempelvis sjösänkningar och anläggande av vattenkraftverk, har minskat förekomsten. Idag finns malen endast kvar i fyra ursprungliga områden: Båvenområdet, Emån, övre delen av Helge å  och nedre delen av Helge å. Utöver dessa är mal känd från ett fåtal andra sjöar, varav de flesta är illegala utsättningar.    Hotbilden är idag fragmentering och isolerade bestånd då många vattendrag och sjösystem är påverkade av vattenkraft och andra dämmen, vilka hindrar malen från att sprida sig till fler och större områden. Sjösänkningar, rensningar av vattendrag och annan verksamhet har inneburit och innebär än idag att lämpliga lekmiljöer och uppväxtområden försvunnit. Genetiska undersökningar visar att malpopulationerna i Sverige har låg genetisk variation och att det troligtvis är få individer som deltar i leken, vilket talar för att antalet lekhabitat är en begränsande faktor idag.   I den svenska rödlistan från 2015 klassas malen som Sårbar (VU). Malen är fredad från fiske enligt 2 kap. 5 § i förordningen (1994:1716) om fisket, vattenbruket och fiskenäringen.   Målet med programmet är att förstärka bestånden genom åtgärdande av vandringshinder samt översyn och anpassning av reglering. Andra viktiga åtgärder är olika biotopförbättrande åtgärder, exempelvis gynnade av strandnära vegetation och test av konstgjorda leknästen. Utöver detta finns ett stort fokus på förbättrat kunskapsunderlag och informationsspridning.    De åtgärder som förutsätts finansieras av Havs- och vattenmyndighetens medel för genomförande av åtgärdsprogram för hotade arter beräknas totalt uppgå till 5 875 000kr under programmets giltighetsperiod 2017– 2021.This action program aims to improve the status of the European catfish (Siluris glanis) in Sweden. It is an indicative, but not legally binding, action program.    The European catfish migrated to Swedish lake and river environments during the Ancylus lake period, an era when the temperature was higher than today. The species is the largest freshwater fish in Sweden with a record measuring 3.6 meters standard length and an estimated weight of about 180 kg. It is considered to be nocturnal and an opportunistic predator eating both fish and other freshwater organisms, such as amphibians, birds, crayfishes, insects, worms and molluscs. The species require relatively high water temperatures to spawn, which means it is not reproducing every year in Swedish waters.    The European catfish is listed as Vulnerable (VU) on the Swedish red list. Four natural populations exist, all located in the southeast of Sweden, in the water systems Nyköpingsån (lake Båven), Emån, the upper part of Helge å and the lower part of Helge å. Additional records are known from a few other lakes, all results of illegal releases.    The main reason for the decline is destruction of suitable habitat, such as large lowland rivers with a natural river environment. These habitats have been severely affected by human interference from the 19th century onwards, such as drainage of wetlands, water regulation, diversion of water, and physical impact on shore and bottom habitats.    Genetic studies show that the populations in Sweden are genetically unique, but have low genetic variation indicating that the number of spawning individual is low, possibly due to lack of suitable spawning habitats.  The European catfish is protected from fishing in Sweden. Other important measures is to make suitable habitats available by review and adjustments of legislation and water regulations in force. Also to improve the biotopes, for example promote the access to suitable spawning habitats and experiments with artificial nests. In addition, there is a great focus on an improved knowledge base and dissemination of information.   The cost for the conservation measures, to be funded from Swedish Agency for Marine and Water Management allocation for action plans is estimated at 580 000 € during the period 2017-2021.Citat från förordet: "Jan Eric Nathanson, tidigare vid SLU, Institutionen för akvatiska resurser, Sötvattenslaboratoriet har bidragit med underlag till programmet. Förankring av åtgärderna har skett i samråd och en bred remissprocess där statliga myndigheter, kommuner, experter och intresseorganisationer haft möjlighet att bidra till utformningen av programmet."</p

Antipredator phenotype in crucian carp altered by a psychoactive drug

Predator-inducible defenses constitute a widespread form of adaptive phenotypic plasticity, and such defenses have recently been suggested linked with the neuroendocrine system. The neuroendocrine system is a target of endocrine disruptors, such as psychoactive pharmaceuticals, which are common aquatic contaminants. We hypothesized that exposure to an antidepressant pollutant, fluoxetine, influences the physiological stress response in our model species, crucian carp, affecting its behavioral and morphological responses to predation threat. We examined short- and long-term effects of fluoxetine and predator exposure on behavior and morphology in crucian carp. Seventeen days of exposure to a high dose of fluoxetine (100 mu g/L) resulted in a shyer phenotype, regardless of the presence/absence of a pike predator, but this effect disappeared after long-term exposure. Fluoxetine effects on morphological plasticity were context-dependent as a low dose (1 mu g/L) only influenced crucian carp body shape in pike presence. A high dose of fluoxetine strongly influenced body shape regardless of predator treatment. Our results highlight that environmental pollution by pharmaceuticals could disrupt physiological regulation of ecologically important inducible defenses

Experimental manipulation of perceived predation risk and cortisol generates contrasting trait trajectories in plastic crucian carp

Most animals constitute potential prey and must respond appropriately to predator-mediated stress in order to survive. Numerous prey also adaptively tailor their response to the prevailing level of risk and stress imposed by their natural enemies, i.e. they adopt an inducible defence strategy. Predator exposure may activate the stress axis, and drive the expression of anti-predator traits that facilitate survival in a high-risk environment (the predation-stress hypothesis). Here, we quantified two key morphological anti-predator traits, body morphology and coloration, in crucian carp reared in the presence or absence of a predator (pike) in addition to experimental manipulation of physiological stress via implants containing either cortisol or a cortisol inhibitor. We found that predator-exposed fish expressed a deeper-bodied phenotype and darker body coloration as compared with non-exposed individuals. Skin analyses revealed that an increase in the amount of melanophores caused the dramatic colour change in predator-exposed fish. Increased melanization is costly, and the darker body coloration may act as an inducible defence against predation, via a conspicuous signal of the morphological defence or by crypsis towards dark environments and a nocturnal lifestyle. By contrast, the phenotype of individuals carrying cortisol implants did not mirror the phenotype of predator-exposed fish but instead exhibited opposite trajectories of trait change: a shallow-bodied morphology with a lighter body coloration as compared with sham-treated fish. The cortisol inhibitor did not influence the phenotype of fish i.e. neither body depth nor body coloration differed between this group and predator-exposed fish with a sham implant. However, our results illuminate a potential link between stress physiology and morphological defence expression

Sex matters : predator presence induces sexual dimorphism in a monomorphic prey, from stress genes to morphological defences

Inducible defences allow prey to increase survival chances when predators are present while avoiding unnecessary costs in their absence. Many studies report considerable inter-individual variation in inducible defence expression, yet what underlies this variation is poorly understood. A classic vertebrate example of a predator-induced morphological defence is the increased body depth in crucian carp (Carassius carassius), which reduces the risk of predation from gape-size limited predators. Here, we report that among-individual variation in morphological defence expression can be linked to sex. We documented sexual dimorphism in lakes in which crucian carp coexisted with predators, where females showed shallower relative body depths than males, but not in a predator-free lake. When exposing crucian carp from a population without predators to perceived predation risk in a laboratory environment (presence/absence of pike, Esox lucius), we found that males expressed significantly greater morphological defence than females, causing sexual dimorphism only in the presence of predators. We uncovered a correlative link between the sex-specific inducible phenotypic response and gene expression patterns in major stress-related genes (POMC, MC3R, and MC4R). Together, our results highlight that sex-specific responses may be an important, yet underappreciated, component underlying inter-individual differences in the expression of inducible defences, even in species without pronounced sexual dimorphism

More than meets the eye : Predator-induced pupil size plasticity in a teleost fish

Most animals are visually oriented, and their eyes provide their ‘window to the world’. Eye size correlates positively with visual performance, because larger eyes can house larger pupils that increase photon catch and contrast discrimination, particularly under dim light, which have positive effects on behaviours that enhance fitness, including predator avoidance and foraging. Recent studies have linked predation risk to selection for larger eyes and pupils, and such changes should be of importance for the majority of teleost fishes as they have a pupil that is fixed in size (eyes lack a pupillary sphincter muscle) and, hence, do not respond to changes in light conditions. Here, we quantify eye and pupil size of individual crucian carp, a common freshwater fish, following controlled manipulations of perceived predation risk (presence/absence). We also tested if crucian carp responded to increased predation risk by shifts in diel activity patterns. We found that crucian carp show phenotypic plasticity with regards to pupil size, but not eye size, as pupil size increased when exposed to predators (pike). Predator-exposed crucian carp also shifted from diurnal to nocturnal activity. Using a modelling exercise, we moreover show that the plastically enlarged pupils significantly increase visual range, especially for small objects under dim light conditions. Overall, our results provide compelling evidence for predator-induced pupil enlargement resulting in enhanced visual capabilities in a teleost fish. Pupil size plasticity in combination with the observed shift towards nocturnal activity may allow for efficient foraging also under dark conditions when predation risk from diurnal and visually oriented predators is reduced. The data highlight the powerful role of predation risk for eye development and evolution

SR_2017

The data included in this directory was used for analysis in the publication "A predation cost to bold fish in the wild"