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The importance of predation, cannibalism and resources for production and abundance of crayfish Karin Olsson Introductory paper No. 164 Supervisor: Per Nyström Department of Ecology Ass.Supervisor: Wilhelm Granéli Institute of Limnology Lund University Lund 2005 Cover picture: Taken by K. Olsson, New Zealand 2003. The picture is a small detail on a Maori totem pole. 2 CONTENT 1. SUMMARY.......................................................................................................................3 2. FACTORS AFFECTING ABUNDANCE AND GROWTH ............................................5 2.1 ABIOTIC FACTORS ..........................................................................................................5 2.2 ABIOTIC FACTORS AFFECTING CRAYFISH .........................................................................7 2.3 RESOURCES .................................................................................................................11 2.4 CRAYFISH UTILIZATION OF FOOD RESOURCES ................................................................14 2.5 PREDATION ..................................................................................................................17 2.6 CRAYFISH AS PREY, PREDATOR AND CANNIBAL .............................................................21 3. ENERGY FLOW IN BENTHIC FOOD WEBS.............................................................26 3.1 TOP-DOWN AND BOTTOM-UP ........................................................................................28 3.2 THE IMPORTANCE OF CRAYFISH IN FOOD WEBS ..............................................................28 3.3 INVADING CRAYFISH AND THE LOSS OF NATIVE CRAYFISH .............................................30 4. PROPOSED RESEARCH ............................................................................................33 4.1 FIELD STUDY 1.............................................................................................................33 4.2 ENCLOSURE EXPERIMENT .............................................................................................33 4.3 POOL EXPERIMENT 1, 2 AND 3 ......................................................................................35 4.4 FIELD STUDY 2.............................................................................................................36 4.5 TIME PLAN ...................................................................................................................36 5. ACKNOWLEDGEMENT ...............................................................................................36 6. REFERENCES ..............................................................................................................37 3 1. Summary “The crayfish is a small, freshwater, lobster-like creature which in nature inhabits ponds, streams and rivers.”(Groves, R.E. 1985). Crayfish are often regarded as keystone species in freshwater systems and they can in many cases dominate the benthic biomass. As they are omnivorous they can have an impact on several trophic levels and their role in the food web is rather complex. Crayfish have the ability to act as herbivores, detritivores and predators. This polytrohic behaviour is rather unique in freshwater ecosystems. Several studies have shown that crayfish can have strong impacts on other benthic organisms through direct and indirect effects. Crayfish can for example totally exclude some species of macrophytes due to intensive grazing. They have also been shown to alter the invertebrate composition in streams and lakes due to selective predation. In most studies they are regarded as cannibalistic and are potentially able to influence their own population dynamics. However, there are few studies from the nature supporting this cannibalistic behaviour and it might not be as common as previously thought. Crayfish certainly play an important role as prey for many species, such as predatory fish, wading birds and some mammals. In their natural habitats crayfish often face a multipredatory situation and how this affects the behaviour, growth and abundance of crayfish is not fully understood. Signal crayfish (Pacifastacus leniusculus) and noble crayfish (Astacus astacus) are the two species found in Swedish freshwaters today. Noble crayfish is regarded as the only native species in Scandinavia and in Sweden it has been stocked in lakes and streams for the past 500 years (Skurdal et al. 1999). Noble crayfish had earlier its main distribution in southern parts of Sweden, but today it is spread in most parts of the country (fig. 1). Signal crayfish, which originate from North America, was introduced in Sweden in the1960s to compensate for the drastic decline of noble crayfish populations in southern Sweden caused by the crayfish plague (Skurdal et al. 1999). It has been stocked into large parts of southern Sweden, and can be found up to Dalälven river system. 4 Northern boundary for signal crayfish Figure 1. The distribution of noble crayfish in Sweden. From Skurdal et al. 1999. The two species are ecologically similar in many ways but there are also differences that may influence their abundance and interactions with other trophic levels. They are similar in size, morphology and life history, and their life cycles are synchronous (Abrahamsson 1971, Söderbäck 1995). They are both omnivorous feeders with a nocturnal activity pattern and seem to prefer the same type of biotope (Abrahamsson 1983). It has been shown that they are able to mate with each other but that it only results in sterile eggs (Söderbäck 1994). It was also shown that noble females had a higher degree of mating with signal males than signal females with noble males, which resulted in fewer offspring in the noble crayfish population than the signal crayfish population (Söderbäck 1994). The signal crayfish is a carrier of the crayfish plague and the restocking of signal crayfish has spread the disease to a large part of southern Sweden. Despite of this great change in distribution of crayfish populations and the increasing number of new waters with often very dense crayfish populations, there is little knowledge about the impact of both the introduction of signal crayfish and the loss of noble crayfish on freshwater ecosystem functioning. The signal crayfish seems to grow faster, be more aggressive and have denser populations than noble crayfish. This may lead to a stronger impact on the ecosystem by the introduced species than from the native one (Nyström 2002). If that is true, how have the change from noble crayfish to signal crayfish in Swedish streams and lakes affected the invertebrate composition, resource availability (mostly detritus and 5 algae) and predator regime in these systems? Are there differences between the two species regarding productivity, resource use and abundances in equal environments? Do the same factors regulate signal- and noble crayfish populations? This introductory paper will give a brief description of the knowledge today about these topics and the problems attached to studies on complex systems and the interactions between present organisms. During the reading of loads of articles I have realised that crayfish are good model-organisms, since they are easy to catch and study in nature and they are easy to keep under experimental conditions, and their unique role in ecosystems makes them very interesting to study. Here I try to show their importance, my own thoughts and proposed research. 2. Factors affecting abundance and growth 2.1 Abiotic factors Temperature and light are abiotic factors affecting most species. Their interactions can for example modify the migration response in fish and also activity of invertebrates (Cossette and Rodrígues 2004). At low temperatures the oxygen and carbon dioxide levels are usually high and the reversed for high temperatures which certainly affects most organism living in temperate regions (Coker 1968). Light is very important for foraging success of many consumer species and prey species as well. Some species are adapted to night activity (nocturnal) while others are more active at daytime (diurnal) and some species can switch between these two when necessary for their survival. The acidity of lakes and streams can affect the distribution and abundance of some aquatic animals (Bradford et al. 1998) and one of the most important abiotic factors seems to be pH. Studies have shown that some fish species are not present in streams and lakes with a pH below 6. For example, exposure to pH< 5.0 for a longer time caused mortality in brown trout (Åtland 1998). At low pH levels toxic compounds (e.g. aluminium ions) are mobilised (Sandin 2003) which makes the habitat less suitable for many species. The predominant chemical stressors for fish, and certainly other aquatic animals, are low pH and high aluminium (Al ion) concentrations caused by anthropogenic acidification (Åtland 1998). Physiological effects can be aluminium precipitation on fish gills, disturbed ion regulation and respiratory and circulatory disturbances (Åtland 1998). 6 The animals living in streams face somewhat different abiotic factors than animals in lakes. In streams velocity is a factor that can have great impact on the distribution and abundance of species. Current velocity often present a direct physical force on stream organisms, and also affects substrate composition and oxygen content of the stream (Sandin 2003). In lakes the depth and circulation may be of more importance than in streams. High levels of nitrogen can in some cases promote anoxia at deep water as oxygen is not circulated all way down in lakes all year round, which may lead to decreased diversity since most species are not able to live in areas with low oxygen levels (Deegan et al. 2002). The constant flow of water in streams creates a specific environment where the same water never runs over the same place twice. In the lake, however, the same water can be circulated many times and be “stored” at the same place for longer periods of time. Thus, lake and stream environments are quite different and the animals living there face problems of various kinds. 2.2 Abiotic factors affecting crayfish Crayfish can be found in a diversity of habitats in freshwater environments and are regarded as key species in many lake and streams. Geographical and environmental factors may affect population density, growth and life history of different species but also different populations within the same species (Momot et al. 1978). Physico-chemical (i.e. abiotic) factors sets the limits for crayfish populations based on physiological adaptations (Lodge and Hill 1994). There are more than 500 different crayfish species found globally today and they are present on all continents but Antarctica (Holdich 2002). They have different environmental adaptations and tolerance levels (table 1). Subsequently, the abiotic factors affect on growth, survival and reproduction may be species specific. 7 Table 1. Comparative abilities of some crayfish species of the families Astacidae, Parastacidae and Cambaridae to tolerate different levels of temperature, oxygen concentrations, salinity and hydro period. From Nyström (2002). Species Temperature Temperature Oxygen Oxygen Salinity Ability to (tolerance) (for best (lower lethal (for best (tolerance) survive in (ºC) growth) limit) growth) (ppt) temporary (ºC) (mg-1) (mg-1) habitats Astacidae Astacus astacus <28 16-24 3.2 >5 -- Weak A. leptodactylus 4-32 21.8 3.97 >6 0-14 -- Austropotamobius pallipes <28 21.4 2.7 -- -- Weak Pacifastacus leniusculus <33 22.8 -- -- 0-21 Weak Cherax destructor 1-35 22-30 1.0 >5 0-12 Good C. tenuimanus 4-28 15-22 3.7 >7 0.3-12 Moderate C. quadricarinatus 10-30 25-30 3.0 -- -- Moderate Euastacus armatus <28 -- 3.0 -- -- Moderate Orconectes rusticus 2.5-33 -- -- -- -- Moderate Procambarus clarkii <35 22-30 0.4-1.0 >3 0-12 Good P. kilbyi 1.0-38.4 -- 1.33 -- -- Good P. loenensis 1.0-38.9 -- 1.53 -- -- Good P. paeninsulanus 4.7-37.1 -- 1.72 -- -- Moderate P. spiculifer 8.1-33.3 -- 2.63 -- -- Moderate Parastacidae Cambaridae --: Data not available. Temperature and light The optimum temperature for growth and survival in crayfish seems highly variable and can differ by several degrees between species (Nyström 2002, Whitledge and Rabeni 2003, Paglianti and Gherardi 2004). Temperature regulates several behaviours in crayfish, such as moulting (Whitledge and Rabeni 2003), growth, survival of juveniles and reproduction. For example A. astacus needs at least 3 months of temperatures in excess of 15°C for successful reproduction (Abrahamsson 1966, Abrahamsson 1971) and egg development (Pérez et al. 2003). Drastic changes in temperature can induce moulting failure, which can lead to death in crayfish due to thermal shock (Nakata et al. 2002). Abrahamsson (1966) observed that a cold summer reduced growth in A. astacus compared to normal summer temperatures. At normal temperatures the weight increase was about 31% higher than in the cold years. The metabolic turnover has been showed to increase rapidly in A. astacus between 15 and 20°C (Kristiansen and Hessen 1992). High temperatures seem to be important for high growth rates (Kristiansen and Hessen 1992), but too high temperatures can also be stressful. High temperature (22 ºC) 8 has been shown to increase the mortality in crayfish that had been injected with white spot syndrome virus (WSSV), which indicates that high temperatures can negatively affect the disease pathogenicity in crayfish (Jiravanichpaisal et al. 2004). In temperate regions the growth period is limited to the warmer summer months of the year and the decrease in temperature and light in autumn triggers the start of the mating season (Jonsson and Edsman 1998). The depth distribution of crayfish in lakes may also be temperature dependent. Skurdal et al. (1988) observed that noble crayfish (A. astacus) were restricted to the shallower parts above the thermocline during the summer months. Temperature can also influence the geographical and local distribution (Nakata et al. 2002) and an attempt to introduce Procambarus clarkii into southern Sweden failed probably because the species is adapted to survive in warmer waters (Blindow et al. 1984). Light intensity also affects the behaviour of crayfish and seems to have a subordinated role in regulating reproduction and moulting compared to temperature (Westin and Gydemo 1986). In an experiment conducted by Nyström (1994) it was shown that increased light intensity increased the survival rate of juvenile P. leniusculus. This increased survival could be due to higher food availability (e.g. epiphytic algae) or reduced number of conflicts (e.g. cannibalism) as a result of low activity among the juveniles (Nyström 1994). Calcium, pH and acidity Calcium level is a factor that has been shown to affect growth in freshwater crayfish (France 1987, Hessen 1989). Calcium is stored in the exoskeleton in most crustaceans and used when the crayfish undergoes moulting, so sufficient amounts of calcium are needed after each moult (Rukke 2002). Calcium deficiency will cause crayfish to moult less or prolonged periods of soft exoskeletons, thus make the crayfish more vulnerable to predation (Stein 1977) and cannibalism (France 1987). Low concentrations of calcium may limit growth and production in A. astacus (Hessen et al. 1991) and Rukke (2002) found that the lower limit for juvenile A. astacus was between >0.0 and 1.0 mg Ca l-1. The shed excuvia after a moult can be an important calcium source for animals living in environments with low calcium concentrations and crayfish often eat their own or others excuvia to compensate for lost calcium during moults (Hessen et al. 1991, Rukke 2002). Rukke (2002) showed that A. astacus had a calcium saturation level around 5 mg l-1 and below that complete calcification of the carapace was not obtained. Acidity has been shown to inhibit the uptake of calcium in crayfish (Appelberg and Odelström 1984, Berrill et al. 1985) and pH is an important factor affecting crayfish abundance and growth. pH have been shown to explain more than half of the variation in 9 crayfish densities among streams and, Seiler and Turner (2004) showed that acidification had a negative effect on the growth for individual crayfish but a positive effect on population size. The population size in acidified streams was six fold larger relative to neutral streams. This can probably be explained by decreased predation pressure in the acidified streams and modifications of the food web interactions as fish standing crop decreased in streams with lower pH (Seiler and Turner 2004). In Plastic lake Ontario, USA, it was shown that acidification explained the disappearance of Orconectes virilis from the lake (France and Collins 1993). A suggestion for the drastic decline and disappearance of O. virilis, due to acidification, was a combination of reproductive impairment, hatchling mortality, disruption in recalcification and increased infection by microsporozoans (France and Collins 1993). Lake acidification can cause great reduction in exoskeleton calcification and hardness (France 1987). Acidification (e.g. lowered pH) can lead to increased uptake of trace metals, such as Hg and Mn, in crayfish, which can become toxic to crayfish in interactions with other elements (France 1987). Calcium and carbonate ions are necessary for the calcification of the cuticule and in acidic streams calcium is nearly absent (Seiler and Turner 2004), but still some crayfish can survive, reproduce and have high abundance in those streams (Hill and Lodge 1994, Olsson own observations 2003). How crayfish can cope in these acidic streams is still poorly understood. pH may also affect the oxygen levels in lakes and species with comparatively high oxygen demands, for example A. astacus and P. leniusculus, may suffer high mortality in acidic lakes (Nyström 2002). Lodge and Hill (1994) argue that in some lakes crayfish may not exist due to winterkills, because of anoxic conditions under the ice. However, some species may be able to cope with extreme conditions better than others. For example, P. leniusculus hatch earlier, have a faster growth during the juvenile stages than A. astacus (Söderbäck 1995) and therefore they may be better adapted to cope with the hard winter conditions than A. astacus (Westman et al. 2002). Substrate and temporary habitats One of the most important abiotic factor affecting the abundance of crayfish seems to be bottom substrate (Blake and Hart 1993, Savolainen et al. 2003, Olsson et al. unpublished). Some species of crayfish that lives in temporary habitats caused by floods or drought, have the capacity to burrow into the streambed, such as Cambarus latimanus and Cambarus fodiens (Flinders and Magoulick 2003). These species may not be equally affected by substrate composition as non-burrowing species. For non-burrowing species stream disturbance is more important as floods will force them to abandon their shelters and migrate 10 to pools or up on land, while burrowing species will be able to withstand disturbances (e.g. floods) much better by hiding in sealed burrows (Berrill and Chenoweth 1982, Flinders and Magloulick 2003). Some non-burrowing crayfish species, however, seem to have the ability to become burrowers when the water levels drops below them during drought conditions (Berrill and Chenoweth 1982). For example, in its native habitat in North America P. leniusculus is not regarded as a burrowing species but has become so in some countries were it has been introduced (Vorburger and Ribi 1999). So how important is the substrate for crayfish densities? Even if many crayfish respond to drought conditions or floods by burrowing, the bottom substrate has to be soft enough to burrow into (Taylor 1983). The substrate composition can therefore be important even for burrowing species but in a different way than for non-burrowing species. In a study by Savolainen et al. (2003) the growth in crayfish was improved by using gravel at the bottom compared to bare bottom. In another study the substrate size was the most important factor explaining crayfish (Paranephrops planifrons) abundance in streams without introduced fish (Olsson et al. unpublished). The substrate seems to be important for shelter use and it has been shown to be important for the growth in crayfish. If crayfish are not able to seek refuges, interactions with other crayfish or predators will increase and injuries will be more common. When crayfish loose a chelae or a leg they have to use energy to regenerate the missing part and thus allocate less energy to growth (Savolainen et al. 2003). Lodge and Hill (1994) showed that availability of substrate was a strong factor affecting the population size for crayfish and that lakes that had less than 1520% of the littoral zone occupied by rocky substrate had small crayfish populations. Crayfish also have a great impact on the bottom substrate through burrowing activities and transport of particles and this can cause temporal differences in the flow patterns in streams (Statzner et al. 2003). Salinity Shorter exposure to saline water does usually not cause mortality in freshwater crayfish species (Nyström 2002) but salinity tolerance varies between species and also for populations within the same species. Salinity may be an important distribution-limiting factor for freshwater crayfish but the factor is not well studied (Lodge and Hill 1994). It is known that several species can potentially colonise brackish waters for feeding purposes but may not be able to reproduce and grow in habitats with salinities exceeding 5-7 ppt (Nyström 2002). Pacifastacus leniusculus has been shown to survive in salinity up to 17 ppt (Rundquist and Goldman 1978), and it seems that other crayfish species, such as Austropotamobius pallipes 11 and Astacus leptodactylus, can hatch and develop in moderately saline waters as well (Holdich et al. 1997, Susanto and Charmantier 2000). The importance of abiotic factors in determining crayfish populations varies between crayfish species, and it is hard to draw any general conclusions about the effects of, for example shelter use, acidity and substrate. Abiotic factors has to be considered together with other factors such as interactions between crayfish and other organisms and influences of diet upon crayfish behaviour (Verhoef and Austin 1999). 2.3 Resources All natural waters contain a substantial amount of minerals and all organisms require a certain amount of these, although not necessarily in the same proportion (Coker 1968). Species can have different needs that have to be fulfilled for optimum growth and limited resources can strongly affect the abundance of species. Animals can be regarded as energy processors that acquire energy for maintenance, growth, and reproduction (Yodzis and Innes 1992). To gain this energy several resource requirements of the animal must be met. Resources are not evenly distributed in nature and species can often be found in some habitats but not others. This is due to where the needed resources are present. Use of different habitats can vary seasonally, as different feed is present at different times, and among age classes, as different life stages need different resources (Cossette and Rodríguez 2004). Ideal free distribution (IFD) has been used as a powerful tool to predict and explain the distribution of animals in relation to their resources (Jackson et al. 2004). IFD predicts that individuals will distribute themselves, if equally competitive, between patches of resources such that equilibrium is achieved when the proportion of individuals equals the proportion of available resources in each patch (Jackson et al. 2004). Nutrients are transported in the environment in different ways and in streams there is a horizontal transport while it is a more vertical transport in lakes (Wotton and Malmquist 2001). The nutrient cycling in streams resembles a downstream “spiral” and the spiralling length is used to quantify the nutrient cycling in streams (Essington and Carpenter 2000). Substrate composition and channel type affect the nutrient transport in streams, but these attributes may be site specific and depend on complex interactions between light availability and channel morphology (Essington and Carpenter 2000). In lakes, nutrient cycling is often quantified by calculating the portion of primary production supported by recycled nutrients 12 and cycling is controlled by processes that promote remineralization (Essington and Carpenter 2000). Consumers may have very different roles in the regulation of nutrient cycling in streams and lakes. In lakes, consumers affect the rate of nutrient remineralization from particles and the rate of particle export, while in streams they alter the nutrient cycling by reducing cycling within algal mats, which affects the uptake and export of nutrients (Essington and Carpenter 2000). Different food sources contain different amounts of nutrients, and why some species prefer a certain kind of food is not well understood. The energy gained from the food should be the main reason for eating it and several studies have shown that this is the case for most animals, but there are of course exceptions where less energy ranked food is equally consumed as higher ranked food. Optimal diet will exhibit basic properties according to Lacher et al. (1982), which states: “the decision to select or reject a particular food item should only depend upon the absolute abundance of other food items which convey a greater benefit” and also states that animals will first feed the most preferred food available and than less preferred. 2.4 Crayfish utilization of food resources Crayfish, being omnivorous consumers, feed on a great variety of food items, such as detritus, algae, macrophytes, invertebrates, fish and even other crayfish (Appelberg and Odelström 1984, D’Abramo and Robinson 1989, Momot 1995, Guan and Wiles 1998, Nyström 2002). There are indications of an ontogenetic diet shift in crayfish where adult crayfish have a higher proportion of detritus and plants in their diet, while younger crayfish (i.e. juveniles) feed mostly on invertebrates (Mason 1975, Lodge and Hill 1994, Momot 1995, Nyström 2002). The difference between feeding habits in adult and juvenile crayfish may be a result of slower growth in adult crayfish and adult crayfish therefore need less protein than the fast growing juveniles (Lodge and Hill 1994). Juvenile crayfish often moult more frequently than adult crayfish. For example, juvenile P. leniusculus moult up to 9 times a year, while adults may moult once a year or less (Mason 1975). Number of moults may differ between crayfish species and also within species that lives under different environmental conditions and therefore not only age determines number of moults in crayfish. Adult crayfish may also be less successful as predators than juveniles, as they have slower mobility, and adult crayfish may therefore have less animal matter available to them for consumption (Abrahamsson 1966, 13 Lodge and Hill 1994, Whitledge and Rabeni 1997). Another explanation, proposed by Momot (1995), is that the ingestion of plant material in adult crayfish is due to micronutrient requirements, such as carotenoids. D’Abramo and Robinson (1989) argue that plant tissue appears to be essential for normal pigmentation in crayfish and therefore is an abundant component of the diet. All food items are not equally abundant throughout the year and seasonal variations in diets are common among crayfish species (Abrahamsson 1966, Guan and Wiles 1998). For example A. pallipes had more detritus in their guts during autumn when leaf-fall is frequent, moss was mostly found in summer and insect larvae increased during spring and summer seasons when their biomass are greatest (Gherardi et al. 2004). Guan and Wiles (1998) showed that animal food was the main diet of crayfish in summer (about 30% of the total dietary wet weight). They further agreed with Momot (1995) that animal food is the most important food source for crayfish since the summer is the most important season for feeding. Food availability can be of great importance for crayfish growth, activity and number of mature females and food shortage can also have a severe affect on crayfish cannibalistic behaviours (Nyström and Granéli 1996). Guan and Wiles (1998) also found fragments of crayfish in their gut content analysis, which originated from both predated crayfish and from crayfish own exoskeletons. Preferences Different food items clearly have different energy content and the same food items can also vary in energy content, as energy can be located in different ways. For example alder leaves contain almost twice as much nitrogen than maple leaves. Crayfish show a preference for particular leaf species (Mason 1975) due to for example different toughness in leaves, which makes some leaves more easily consumed even if they contain less energy. The macroalgae, Chara, has a relatively low energy value compared to other macrophytes, still they are preferred by crayfish (Momot 1995, Nyström and Strand 1996). This can be explained by the fact that Chara has low amounts of cellulose and therefore is easier to process. It may also be easier to handle (digest) Chara than floating and semi buoyant macrophytes and it might serve as a calcium source for crayfish (Momot 1995). Another explanation to crayfish grazing on Chara can be that it develops dense mats containing microscopic plants (e.g. periphyton) and animals in great amounts, which can be of energetic (protein) value for the crayfish (Momot 1995). The diet of crayfish is certainly also dependent on the habitat they live in. 14 Parkyn and Collier (2000) showed that crayfish in native forest streams consumed more detritus (62%) than invertebrates (23%) and that the case was reversed in pasture streams were crayfish consumed more invertebrates (42%) than detritus (25%). Plant tissue and detritus have often been shown to be the dominant food item in guts (Abrahamsson 1966, Momot et al. 1978, Appelberg and Odelström 1984, Whitledge and Rabeni 1997). Detritus, algae and plant tissue are regarded as low quality food because of their low protein content. A protein content of about 30-35% is optimum for crayfish growth (Lodge and Hill 1994). Interestingly, Gherardi et al. (2004) showed that even if crayfish could choose between different food items, they preferred moss (Fontinalis antipyretica) with low protein content compared to the protein richer insect larvae (Ephemeroptera, Tricoptera,and Plecoptera). Carbon in moss was, however, better assimilated compared to carbon in insect larvae, which may explain the preference for the lower quality food by crayfish. In the same study it was shown that fish had the highest protein content and assimilation efficiency of both carbon and nitrogen for the crayfish. Still the crayfish in the study preferred insect larvae to fish and moss over insect larvae. This contradicts Momots (1995) opinion “that crayfish, given a choice, select an animal diet in preference to other alternatives, such as plants and detritus”. If they would prefer fish over moss was however not tested in the study of Gherardi et al. (2004). Whitledge and Rabeni (1997) showed that moss were abundant in all their study streams but still it did not account for a large component in crayfish diet. Nevertheless, laboratory studies have shown that crayfish prefer animal food to live plant material (Ilheu and Bernardo 1993). The preference for benthic invertebrates and dead fish in the study by Ilheu and Bernardo (1993) indicates that the cost involved in foraging on mobile (i.e. fish and fast swimming invertebrates) prey is to high, and therefore less nutritious food are preferred. Nyström et al. (1999) showed that crayfish reduced the abundance of primary consumers, especially snails, due to their low mobility and large size compared to small and fast swimming invertebrates. A similar result was obtained by Stenroth and Nyström (2003) where slow moving organisms, such as leeches, dragonflies, caddisflies, isopods and molluscs, declined in enclosures with crayfish, while more mobile organisms, such as chironomids, stoneflies and trout fry, were less affected by the presence of crayfish. It has been pointed out that crayfish can have strong impact on invertebrate essamblages in lakes and streams (Charlebois and Lamberti 1996). In New Zealand, Usio and Townsend (2002, 2004) found that crayfish selectively preyed upon large and sedentary invertebrates, such as Tanypodinae larvae, which in turn favoured small chironomidae larvae that are a common 15 prey for Tanypodinae. In the study streams where crayfish were abundant, invertebrates like snails and cased caddisflies were rare, due to crayfish predation (Usio and Townsend 2002). As one can see, there is an ongoing debate weather crayfish should be regarded truly as omnivorous, and also if detritus really is of low quality. Some authors consider detritus as nutritional, because it is associated with bacteria and fungi that alter its composition. Crayfish production connected with feeding on plant detritus may be derived from the microbes rather than the detritus itself (Whitledge and Rabeni 1997). Paglianti and Gherardi (2004) showed that, under experimental conditions, juveniles of both P. clarkii and A. pallipes grew faster when fed animal diet than a detritus-based diet. They also showed that if crayfish was only fed animal diet both crayfish species became extremely pale, while the crayfish fed on detritus maintained a normal pigmentation. This indicates that crayfish need both detritus and animal protein in their diet and as D’Abramo and Robinson (1989) states “ it is generally best to feed on a mixture of animal and plant proteins in order to achieve nutritional balance”. It is hard to draw conclusions of crayfish optimal diets for growth and survival because we have limited knowledge on crayfish needs. Another problem is that different species and even individuals of the same species behave differently and may have different needs. Nyström (1999) and Nyström et al. (1999) showed that P. leniusculus had a higher weight-specific consumption rate than A. astacus, which can explain the faster growth in P. leniusculus and this may be the reason for why they reach maturity earlier than A. astacus. Further, results based on stomach analysis are usually underestimating animal food sources due to rapid digestion rates, and slower assimilated food items will be more evident (Momot 1995, Whitledge and Rabeni 1997). Stable isotopes of carbon and nitrogen can provide more accurate estimations of longterm diets, as they reflect the actual assimilation of organic matter into consumer tissue and not only the consumption on a specific occasion (Whitledge and Rabeni 1997, Nyström 2002, Hollows et al. 2002). 2.5 Predation Predation as a structuring force has been the subject of many field studies in freshwater environments (Diehl 1992). If the abiotic requirements and the food supply are good, predation can still decrease or even exclude a prey population from a suitable habitat. Predators can have direct and indirect effect on their prey and also have both negative and positive effects on populations (Resetraits 1991). Predatory fish may, for example, preferentially prey on large predatory invertebrates, thus decreasing the predation pressure on 16 invertebrate grazers (Diehl 1992). The predatory fish in this case has a direct negative effect on the large invertebrates and a positive indirect effect on the small invertebrates, thus changing the abundance and biomass of large and small invertebrates (Diehl and Kornijów 1998). Both direct and indirect effects of predators can cause higher mortality among prey species. Predacious fish have been shown to have direct and indirect effects on the function of detrivores, their efficiency of litter processing and benthic diversity (Nyström et al. 2003, Zhang et al. 2004). Multiple predators All interactions between species are mediated by traits (e.g. life history, morphology, behaviour) and any given species exhibits several types of traits, each which can mediate interactions with other species (Turner et al. 1999, DeWitt and Langerhans 2003). Prey often face multiple-predators in their natural habitats (Resetraits 1991, Sih et al. 1998, DeWitt and Langerhans 2003). The combined effect is seldom the sum of the single effects, i.e. a nonadditive effect (fig. 2), because of the interactions among the predator species themselves (DeWitt and Langerhans 2003), or risk enhancement for prey. A B C C A B C Figure 2. Multiple-predator effect with two predators (A and B) and one prey (C) (after DeWitt and Langerhans 2003). Predator-predator interactions may affect the intensity and profile of the predation pressure experienced by prey (Resetraits 1991). Both predators may, because of the interaction, affect the prey less than if they were the only predator present. When one predator is superior to the other, the less favoured predator may be of no risk to the prey and instead become a prey itself for the superior predator and a competitor for shelter with the prey. Prey responses to predators Optimal foraging and avoiding predation are incompatible goals for prey (Tomba et al. 2001) and many prey are capable of assessing predation risk and use that information to make decisions regarding foraging, activity patterns, habitat selection and refuge use (Turner 2004). 17 A reduction in foraging effort of consumers, induced by higher predation pressure, can result in higher resource availability (Nyström and Åbjörnsson 2000, Bernot and Turner 2001). Predation risk can force consumers to be more prudent in their consumption of resources, which can have a positive effect for consumers if resources have been overgrazed (Turner 2004). Studies on the non-lethal effects of predation on prey growth have generated different results, some showing a large reduction in prey growth (Peckarsky et al. 1993), while others have found small, no or positive effect on the growth (Peacor 2002). Organisms have many different strategies to avoid predation (Tomba et al. 2001) and the use of chemical cues and refuge is widespread among freshwater organisms. Chemical cues can be used both to detect the presence of a predator and to detect potential food resources (Tomba et al. 2001). Prey has been showed to be able to distinguish between different types of predators and respond behaviourally depending on which predator is present (Turner et al. 1999). Avoiding predation is only one of many ways to manage the trade-off between mortality and growth (Tomba et al. 2001), and factors such as food availability, population density (Turner 2004) and abiotic factors are also important for individuals when making their decisions. Reduction in activity and shifts in habitat use by prey certainly influence predation rates (Sih and McCarthy 2002) and predators often have the ability to shift from being selective (consume prey that is most conspicuous and most rewarding) to be generalists (feed on the most abundant prey) (Holt and Polis 1997, Gliwicz 2002). In the presence of predators prey may, besides changing their behaviour, also alter their life history (Brönmark and Vermaat 1998). Lakes vs. streams Perch is one of the most widespread fish species in Sweden and has been shown to be one of the most important predators on crayfish (Svensson 1993, Nyström et al. unpublished). Trout is one of the most important predators on crayfish in streams, even if several other fishes affect crayfish as well, such as eel and pike (Nyström et al. unpublished). In lakes it has been shown that cobble (diameter 64-256 mm) substrate are important as shelter and nursery habitat for crayfish (Stein 1977, Garvey et al. 2003) and most crayfish are found in the littoral areas of lakes. In streams, cobble also seem to be important as refuge, but large crayfish tend to occur in deep water and small ones in shallow areas (Butler and Stein 1985, Rabeni 1985, Englund and Krupa 2000). Predators, in general, are regarded to have strong effect on local prey densities and in lakes this seems to be the case. In streams, however, the pattern is not so clear and some studies have shown that predators have little or no effect on prey densities (Sih and Wooster 1994). Prey, in streams, often use drift as an escape mechanism, but as predators 18 such as trout are visual hunters the drift will only increase the risk of being detected. In lakes, drift is not an option and seeking shelter is a more common escape pattern. Therefore, one could argue that cobble substrate should be more important in lakes than in streams for many prey organism. Large crayfish is not able to drift in the same way as small juveniles and therefore can cobble be of great importance in streams as well. Intra guild predation Intra guild predation (IGP) is predation of species that use similar resources and are thus potential competitors (Polis et al. 1989, Polis and Holt 1992). In theory, the IG prey is often a specialist on the basal resource and more effective in exploiting that resource than the IG predator (Holt and Polis 1997). If the resource is available in huge amounts the competition for the shared resource is low and no IGP is present, but if the density of IG prey is high and therefore the available resource low the shift to become an IG predator by the less competitive species will occur (Polis et al. 1989, Holt and Polis 1997). A study in a Canadian lake showed how the introduced red shiners decreased the rainbow trout population by competition with young trout, even if large trout benefited from the introduction by eating the shiners (Polis et al. 1989). Differences in the dynamics, growth, survivorship, and resource use within age classes of interacting populations are often produced by the combined effect of competition and predation (Polis et al. 1989). This shows that it is often hard to study population dynamics since very complex interactions work at different levels in populations. Cannibalism Cannibalism, where individuals of the same species eat each other, can be regarded as one type of IGP (fig. 3) (Claessen et al. 2003). Cannibalism may influence population structure, life history, competition for mates and resources, and behaviour in many species (Polis 1981, Polis et al. 1989, Elgar and Crespi 1992) and seems to be common in natural environments. Often it is the smaller conspecifics that are eaten and in general the larger (older) animals are more cannibalistic than the smaller (younger) ones (Polis 1981, Elgar and Crespi 1992). 19 Adult predator A Primary consumer Juvenile predator A Resource Figure 3. IGP in a three-species food web with an age-structured species whose juveniles potentially compete with the consumer and whose adults eats the consumer and also can cannibalise on the juvenile as well as compete for the shared resource (modified after Polis and Holt 1992). Cannibalism is often a result of limitations in food availability due to high densities of competitors for the shared resources and lack of alternative food (Elgar and Crespi 1992). When hunger level increases in for example flatworms, predaceous insects, birds, rodents and a lot of other animals, hunger stimulates the cannibalistic behaviour in these species (Polis 1981). Food stress (low availability) increases foraging activity and this increased activity leaves animals more vulnerable to cannibalism by conspecifics. Consumers should expand their diet beyond the normal limits of acceptable prey during periods of hunger or low levels of food, which may include cannibalistic behaviour (Polis 1981). Dominant age classes of large (giants) conspecifics can suppress the recruitment for many years due to eating nearly all eggs and/or young produced by the population (Polis 1981, Dercole and Rinaldi 2002) which indicate that cannibalism can be a very important structural force in population dynamics. Higher densities of individuals within a population may lead to crowding, which force smaller individuals to habitats inhabited by larger ones and thus make them more vulnerable to predation by large conspecifics (Polis 1981, Claessen et al. 2003). When conspecifics are eaten the predator not only gain energy but often also decreased intraspecific competition and increases the per capita food level (Polis 1981, Claessen et al. 2003). For populations that live in environments characterized by large fluctuations in food resources, cannibalism can act as a “lifeboat strategy” to decrease the probability of extinction and to increase the long-term persistence of the population (Polis 1981). Not surprisingly most studies on cannibalism have been assuming high densities, but cannibalism may also be an important factor at low densities (Polis 1981). Another problem in 20 studies of cannibalism among populations is how the measurement is done. Duntil et al. (1997) measured cannibalism in terms of mortality of prey as well as missing legs, injuries and total wet weight of surviving crabs, while others define cannibalism as killing and eating all or part of conspecifics (Elgar and Crespi 2002). As it is hard to extrapolate experimental studies to natural conditions the need for field studies on cannibalism are of great importance to get a better understanding of the importance of cannibalism for population dynamics. 2.6 Crayfish as prey, predator and cannibal Crayfish face many different predators in their natural habitats and predators can have significant effects on growth and abundance of crayfish. Different predators have different lethal and non-lethal impacts on crayfish and as crayfish often face multiple predators in nature their response may vary a lot. There is strong evidence that small crayfish (juveniles) are more vulnerable to predation than large (adult) ones (Stein 1977, Butler and Stein 1985, Svensson 1993, Elvira et al. 1996, Englund and Krupa 2000, Garvey et al. 2003). Garvey et al. (2003) showed that small crayfish were selected by predatory fish (largemouth bass, yellow perch and rock bass) even though large crayfish were more prevalent and many fish species are size-selective to minimize handling cost (Stein 1977) or due to gape-limitations. Prey must be large enough to see and small enough to handle, but also generate an energetic return for the predator (Stein and Magnuson 1976). This selective predation on crayfish, certainly have an impact on the size distribution in crayfish population (Garvey et al. 1994) and can influence crayfish interactions with other organisms and their behaviour. Predators on crayfish Fish, such as eels, pike and perch, are common predators on crayfish, and may affect crayfish through direct predation and by inducing antipredator behaviours (Svensson 1993, Elvira et al. 1996, Blake and Hart 1995). Perch may be more active hunters than eels, which often use a sit-and-wait strategy, and in a study by Blake and Hart (1995) perch ate juvenile P. leniusculus at higher rates than did eels. Nyström et al. (unpublished) found that large perch consumed almost all size-classes of crayfish, even adults, but that young-of-the-year (YOY) crayfish were never found in perch guts. Eels seem not to be restricted in their predation of crayfish by size due to the ability to break, pull and shake their prey (rotational feeding) (Blake and Hart 1995). In Scandinavia, eels are regarded as the most efficient predators on crayfish, probably due to its preference for shallow waters and few prey limitations (Svärdson et al. 1991). Crayfish have been showed to be a large proportion of the diet of otters (Rui Beja 21 1996) and for many bird species as well. Otters consumed most crayfish in spring and summer when the occurrence of large crayfish (>7.0 cm total length) was greatest (Rui Beja 1996), which indicates that otters have a preference for large crayfish. Even invertebrates (i.e. dragonfly larvae, Aeshna grandis) have been shown to prey on YOY crayfish (i.e. Astacus astacus) under experimental conditions (Jonsson 1992). In one of the aquaria, used in this experiment, fifteen out of 25 YOY crayfish had been consumed by Aeshna larvae within 24 hours. If large predatory invertebrates are important predators on YOY crayfish in natural environments is less well known. One important “predator” is man. Every year around 247282 tons of signal crayfish (P. leniusculus) and around 46-58 tons of noble crayfish (A. astacus) are caught in Sweden (Ackefors and Török 2000). Only crayfish larger than 9 cm total length are taken, which potentially could affect the size distribution of crayfish populations in Swedish lakes and streams. If we have a lake where there is a high predation pressure from predatory fish on small crayfish (< 5 cm) and a high predation pressure from humans on large crayfish (> 9 cm) it may lead to a stunted population. Crayfish between 5-9 cm will be less vulnerable to predation and this size refuge can lead to skewed size distribution in the population (fig. 5). Predation pressure High Size distribution Low 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Crayfish size (cm) Figure 5. Predation pressure and size distribution of crayfish in an hypothetic lake with several predators, such as fish, mink and humans. Behavioural effects Crayfish avoid predators by seeking shelter and several studies have shown that crayfish use chemical cues to detect the presence of predators (Blake and Hart 1993, Shave at al. 1994). In response to a predatory attack, crayfish rapidly swims backwards by repeated flexions of the abdomen (tail-flips) and both visual and mechanical stimuli induce this behaviour in crayfish (Wine and Krasne 1972). Avoidance behaviours may be costly for crayfish and has been 22 shown to reduce growth, due to reduced feeding opportunities (Stein and Magnuson 1976, Resetraits 1991, Hill and Lodge 1999). Predatory fish are probably the most important predators on crayfish by affecting survival, growth, distribution and abundance of crayfish in lakes and streams (Nyström 2002), but other predators (terrestrial and invertebrates, including other crayfish) may also be capable of affecting crayfish abundance. Studies have shown that crayfish change their habitat preferences in the presence of predators and Stein and Magnuson (1976) showed that in the presence of fish, small crayfish preferred pebble substrate to sand as it provides better shelter. Blake et al. (1994) showed that weed habitats increased juvenile crayfish survival and growth as weed provided them not only with shelter from a small cyprinid, but also with food. They also showed that the activity of all sizes of crayfish was reduced in the presence of cyprinids, but large crayfish were less affected than small ones. Gelwick (2000) showed that crayfish in response to largemouth bass (Micropterus salmonides) increased their use of shelter and occupancy of deeper water. Largemouth bass were able to consume 50-60% of crayfish in streams were there was no other prey species present. In a study by Englund and Krupa (2000) it was shown that predatory fish affected the depth distribution of different size-classes of crayfish. Small crayfish were more vulnerable to predation in deep water and therefore increased their use of shallower habitats. Large crayfish (> 50 mm body length), however, were in a size refuge and were not consumed even by the largest fishes (120-190 mm). Terrestrial predators, such as mink, raccoons and herons are able to forage in the shallow areas and their efficiency decreases quickly with depth (Englund and Krupa 2000). This might drive larger crayfish to deeper water where they are safe from predation from terrestrial predators, which prefer larger prey and therefore posses a bigger threat to large crayfish than to small ones. Non-predatory fish can also affect growth and survival of crayfish, as they might respond behaviourally to the fish by reducing their activity or by competition for food or shelter by the non-predatory fish (Blake et al. 1994, Gelwick 2000, Barki et al. 2001). If a crayfish is out competed from a patch it should move and occupy another habitat. However, this seems not to be the case with Astacus astacus, which instead seem to stay in the outer region of the original patch, which is less productive (Westman and Savolinen 2001). This could lead to decreased growth and survival for A. astacus when co-occurring with competing species such as nonpredatory fish or other superior crayfish species (e.g. Pacifastacus leniusculus) (Westman and Savolinen 2001). P. leniusculus is regarded as being more aggressive than most other crayfish species (Skurdal et al. 1999). Studies have shown that they have a very flexible body and can 23 turn the cephalothoraxes more than 90° and use their chelae to defend themselves against attacks from the behind (Guan and Wiles 1997). Svärdson et al. (1991) showed that P. leniusculus were better at escaping predation from mink due to a more rapid escape run backwards than A. astacus. Mink is a native species in North America but is introduced in Sweden, which may explain that P. leniusculus is better adapted to this predator than A. astacus. Aggressive behaviour and morphology advantages can decrease the predation pressure and have a positive influence on growth and abundance of prey species. The importance of these factors are not very clear and further studies on species with different behaviours towards predators is necessary to get a better understanding of how predation can affect growth and abundance of prey. Crayfish as predators Crayfish act not only as prey for many species, they are also predators on other species, such as fish, amphibians, invertebrates and even other crayfish. Crayfish species have been shown to be effective predators on freshwater snails (Nyström 1999, Turner et al. 1999) and can have significant impacts on snail abundance and species composition in freshwater environments (Weber and Lodge 1990, Lodge et al. 1994). In a study by Turner et al. (1999), crayfish induced snails to move to the surface of the experimental pools to avoid predation from crayfish at the bottom of the pools. Zebra mussel populations have been shown to decrease due to predation by crayfish. In an enclosure experiment Perry et al. (2000) showed that crayfish decreased the zebra mussel densities (58% lower density in crayfish enclosures than in the controls without crayfish) and that small mussels (< 5 mm) were commonly ingested whole, while larger shells were cracked open. Crayfish may have a similar affect on tadpole abundance, which was the case in a study by Nyström and Åbjörnsson (2000) where crayfish affected growth and survival for tadpoles in pools. As crayfish consume and “destroy” large amounts of macrophytes in ponds, which are important as a substrate for amphibian eggs, crayfish can have a strong indirect effect on reproduction in amphibian populations (Nyström 1999). When crayfish act as a predator in the benthic community, they have both direct (lethal) and indirect (non-lethal) effects on organisms in the community. This has been shown in several studies in lakes, but there is less knowledge about the roles of crayfish on the benthic communities in streams. Do crayfish induce the drifting behaviour in invertebrates the same way as many other predators do? What is the most important structuring force from crayfish as a predator on invertebrates, induced drift or consumption? 24 Fish are important predators on crayfish, but several studies have shown that crayfish can act as predators on small fishes (fish fry) and prey on fish eggs (Rubin and Svensson 1993, Savino and Miller 1991). Crayfish may exclude small benthic fishes from streams through competition for shelter and food, but also by attacking and eating small fish species, such as stone loach and bullhead (Rahel and Stein 1988, Guan and Wiles 1997, 1998). Griffith et al. (2004) found that aggressive crayfish reduced the number of juvenile Atlantic salmon using shelters. They did, however, not observe any predation by crayfish on juvenile salmon and there are to my knowledge no observations on crayfish predation on larger fish. Even so, crayfish may by depletion of the benthos and decreasing the overall food availability, affect growth and recruitment for fish species (Charlebois and Lamberti 1996). Crayfish as cannibals In most studies on crayfish they are regarded as cannibalistic (i.e. eats their own relatives). There are, however, few studies that actually evaluate the importance of this behaviour for population dynamics, and in most cases when cannibalistic behaviours have been observed it has been due to density-dependent interactions in unnatural environments. Momot (1993) did not find any cannibalistic behaviour in adult O. virilis on juveniles, and in laboratory studies it has been shown that adults often have problems catching the more rapid moving juveniles (Blake and Hart 1993). Cannibalism in crayfish seems to be dependent on availability of food, competition for shelter and habitat, and the vulnerable stages of recently moulted crayfish. Corkum and Cronin (2004) showed that the contacts among crayfish, even in dense populations, decreased in more complex habitats and they further argued that when food was limited the crayfish may not seek contact and fight less to conserve energy. Westman et al. (2002) argue that fluctuations in annual abundance of crayfish could be a result of cannibalistic predation pressure on newly released juveniles, but also mentions that “there seems, however, to be a lack of studies on the contribution of cannibalism to variations in crayfish populations”. Many authors have stated that adult crayfish are a potential threat for juveniles and points out that cannibalism may regulate populations in lakes. But, as mention earlier in a study by Englund and Krupa (2000), it was shown that adult crayfish occupied deeper water, while juveniles were restricted to the more shallow parts of the lake. If that is common separation between adults and juveniles in natural habitats, adults would not be very cannibalistic on juveniles, but may be a threat to newly moulted adults. Skurdal and Taugbøl (2002) argue that cannibalism in natural crayfish populations is of minor importance as a limiting factor for the abundance of crayfish and that competition and predation will be far 25 more important. But they also argue that in dense populations with few predators and low influence of other regulatory mechanisms, cannibalism can play an important role in regulating densities and recruitment. They also mean that the cannibalistic nature of crayfish can be a useful mechanism to prevent over utilisation of resources and keep down the population on a stable level. Several factors seem to influence the cannibalistic behaviour in crayfish and how important it is in nature remains to be answered. 3. Energy flow in benthic food webs Knowledge of the amounts of energy and nutrients passed between all functional groups will make it possible to construct dynamic food webs (Horne and Goldman 1994). A food web can be made for a specific river or lake when knowledge of the present species and the energy flow between those species are obtained. The transfer of energy and nutrients from one level to another is important for biological success and in general the higher up in the food chain the greater the energy and nutrient content of the food item consumed (Horne and Goldman 1994). This gives that the energy conversion efficiency increases from light to algae to herbivores to primary carnivores to the top predator through complex interactions (Horne and Goldman 1994). Food chain length may be affected by the productivity of the system, but there are different opinions about this relationship (Morin 1999). Omnivory, when a consumer can feed on different trophic levels, will not fit into the simple food chain models and the response to productivity in food webs may differ greatly between models containing omnivores and food web models that ignore omnivory (Oksanen et al. 1981). The energy supply for benthic consumers comes from a diversity of sources and the inputs of different sources vary greatly in space and time, which makes it difficult to fully understand the energy flow and food web relations in benthic communities (Peterson 1999). One important tool for gaining a better understanding is stable isotope analysis. The isotopic ratios of carbon, nitrogen and sulphur in organic matter, producers and consumers have proved to be useful in describing the organic matter flow and food web relationships in aquatic communities (France 1996, Vander Zanden et al. 1997, Peterson 1999, Iken et al. 2001). 3.1 Top-down and bottom-up Abiotic factors, resources and predation all affect the abundance and growth for consumer species in very complex ways. Several models have been developed to explain patterns of abundance and distribution in nature. The most common models are based on the theories of 26 top-down (TD) and bottom-up (BU) impacts on community structure. The combined theory BU:TD predicts that top-down processes (predators) should be strong at the top of the food web and weakens towards the bottom, whereas bottom-up processes (resource availability) should be strong at the bottom and weaken towards the top (McQueen et al. 1989). However, in a study by Gliwicz (2002) on zooplankton it was found that under certain circumstances, the abundance and community structure was regulated by top-down forces and under other circumstances it was regulated from the bottom up (figure 6). (a) PREDATION (b) PREDATION (c) PREDATION Body-size dependent vulnerability Mortality Body-size dependent predation risk ZOOPLANKTON ABUNDANCE AND COMMUNITY STRUCTURE Energy-transfer efficiency and bodysize-related superiority in resource competition FOOD LIMITATION POPULATION DENSITY Reproduction FOOD LIMITATION INDIVIDUAL LIFE HISTORY AND BEHAVIOUR Body-size dependent food-threshold concentration FOOD LIMITATION Fig. 6. Diagrammatic representation of the parity of bottom-up (food limitation) and top-down impacts (predation) on zooplankton abundance and community structure (a), population density and age structure (b), and individual behaviour and life histories (c) (from Gliwicz 2002). Growth rates seem to be controlled from the bottom-up whereas density at both population and community level seems to be controlled from the top-down (Gliwicz 2002). The zooplankton biomass, individual body size and population density can thus be regulated from the top-down by predation and from the bottom-up by available resources, individual growth rate and reproduction (Gliwicz 2002). The strength of the two different controls has been shown to be highly variable. Brett and Goldman (1997) came up with the result that top-down (fish predation) had a much stronger impact on zooplankton biomass than did bottom-up (nutrients) control. Phytoplankton community biomass, however, was more regulated by nutrients (bottom-up). Depending on which organisms we are looking at, the strength of these two process will differ and some factors are of more importance than others. The efficiency of top-down vs. bottom-up forces will also in part depend on the efficiency with which consumers can exploit their prey (Power 1992). Top-down forces in food webs may be 27 modified by the efficiency of consumers that are depending on the interactions among consumers and between consumers and resources (Power 1992). Omnivory effects the dynamics of food webs and probably it is harder to make generalisations about the top-down and bottom-up forces when omnivores are added into the food web. Omnivory diffuses the effect of consumption and productivity across the trophic levels and it also can affect food web dynamics in a way analogous to competition (Polis and Strong 1996). One can argue that omnivory should decrease the strength of interactions in food chains but it is not clear how manipulations in omnivore density would affect lower trophic levels (Brönmark and Vermaat 1998). In lakes, it is suggested that both top-down and bottom-up processes are important, whereas in streams it is suggested that bottom-up processes are most important (Nyström et al. unpublished). Most studies have been done in either open (stream) or closed (lake) systems and comparisons between the two systems are rare (Nyström et al. unpublished). The BU:TD theory gives that in oligotrophic systems the top-down forces may cascade further down the food web than in eutrophic systems (McQueen et al. 1986). In an eutrophic lake a change in piscivore biomass will have little influence at the bottom of the food web, so there will be little or no influence on chlorophyll biomass while the change in piscivore biomass in an oligotrophic lake may have an influence on chlorophyll biomass (McQueen et al. 1989). How BU:TD will affect the abundance, growth and cannibalistic behaviour in omnivores living in oligotrophic lakes compared to those living in eutrophic lakes are not so clear. One question to be answered is if omnivores have different roles in the food web in systems with different nutritional status? 3.2 The importance of crayfish in food webs “Crayfish provide excellent opportunities to study the influence of omnivory and ecosystem engineering in food webs” (Usio and Townsend 2002). The multifunctional feeding habits by crayfish and their multifunctional role in benthic communities as prey and predator makes them unique and gives them a key role in the benthic food web. 28 Multifunctional roles of crayfish in the food web Crayfish play multifunctional roles in many aquatic ecosystems and have significant impact on the biomass and production of lower trophic levels in food web (Lodge and Hill 1994,Whitledge and Rabeni 1997, Nyström 2002, Nyström et al. unpublished). Crayfish can significantly affect the biomass of macrophytes, algae and detritus, but also on biomass and behaviour of several macro-invertebrates (Nyström et al. 2001, Nyström 2002) by consumption and competition. Crayfish play an important role as predators (on invertebrates but occasional on fish as well) and also as shredders (on algae and detritus) in the benthic community (figure 7) (Withledge and Rabeni 1997). Crayfish can consume about 18 times the amount of CPOM (coarse particulate organic matter) estimated to be processed by all other shredders combined (Rabeni et al. 1995). Campostoma spp. Centrarchidae ? ? 1.0 6.0 Benthic algae Scrapers 8.8 5.2 FPOM + microbes 1.7 23.4 2.5 CPOM + microbes Crayfish 63.1 17.9 7.8 3.7 Shredders 7.8 Collectors Predators 68.4 Figure 7. Conceptual model of major energy flow in the Jacks Fork River involving crayfishes and comparison of organic matter consumption and ingestion by crayfish in relation to the rest of the benthic community. All values are in g/m2per year. After Whitledge and Rabeni (1997). In streams and lakes, crayfish often achieve biomass dominance and the basis for this is their efficient exploitation of the benthic fauna (Momot 1995). Because of their large size, polythropy and engineering activities they can drastically affect community members of the benthos, through complex direct and indirect effects (Lodge et al. 1994, Nyström et al. 1999, 29 Usio 2000a, 2000b). The three roles, detritivory, herbivory and carnivory, of crayfish produce a multiple ecosystem impact and the function of crayfish in the total processing of carbon production is in many cases underscored (Momot 1995), which show that they occupy a unique niche in freshwater ecosystems (Momot et al. 1978). Crayfish can as predators on aquatic insects play a significant role in modifying competitive relationships as well as bioenergetic interactions between benthic components of any aquatic community (Momot 1995). Crayfish as ecosystem engineers A dense crayfish population can also have a huge impact on the lake/stream bottom and may stir the bottom layer sufficiently to provide enough oxygenation to release phosphorus and other nutrients that then become available to other organisms in the system (Momot 1995). In a study by Zhang et al. (2004) it was shown that a single crayfish compared to the total benthic biomass in leaf packs, had a much higher physical engineering impact than any other benthic organism in leaf processing. The available amount of detritus and plants is highly variable around the year and in the summer period the FPOM (fine particulate organic matter) generated from crayfish feeding on CPOM may be an important resource for other consumers in the benthic community (Huryn and Wallace 1987). This scenario, when coarse materials are consumed, reduced in size, and egested by crayfish, results in fine particulate material incorporation into the sediment pool. This material is then colonized by microbes and passed through collector-gatherers repeatedly, until it is ultimately flushed from the system (Huryn and Wallace 1987). This processing can enhance seasonal organic matter mineralization, nutrient immobilisation and biomass production within the community (Huryn and Wallace 1987). Without crayfish much of the energy in the food cycle would be “short-circuited” and large amounts of unprocessed CPOM leave the system, leading to decreased energy cycling, community productivity and food availability for other trophic levels in the system (Momot et al. 1978, Huryn and Wallace 1987). 3.3 Invading crayfish and the loss of native crayfish Introduction of exotic crayfish has been done on several places around the world and today introduced species are found on almost all continents (Holdich 2002). In Europe five native species can be found, but there may be more (Lodge et al. 2000, Skurdal and Taugbøl 2002). Four crayfish species have been introduced in Europe and of them the signal crayfish (P. leniusculus) is the most common. It has been introduced to as many as 21 European countries 30 (Holdich 1999). The success of an invader may depend on their ability to adjust to new environments occupied by other crayfish and the success of P. leniusculus can be due to its larger thermal range of tolerance than many other species (Gherardi 2002). P. leniusculus seems to be able to adapt to new environments very well and has been shown to be able to reach a larger size in invaded areas (e.g. Britain) than in its native habitat (Holdich 2002). Behavioural plasticity seems to be a character of successful invasive species, which give them the ability to inhabit a larger range of habitats (Hazlett et al. 2002, 2003). The introduction of P. leniusculus has caused many problems (Holdich 1999) and non-indigenous crayfish species are held responsible for threatening biodiversity in many places around the world (Lodge et al. 2000). The introduced P. leniusculus has been shown to be able to reach higher densities than most native species and consequently exert a larger impact on other biota than the native ones (Skurdal and Taugbøl 2002). Particularly they seem to affect other crayfish species (Söderbäck 1995), benthic fish (Guan and Wiles 1997), molluscs and macrophytes (Nyström et al. 1996, Nyström and Strand 1996). Westman and Savolinen (2001) have been monitoring P. leniusculus and A. astacus in a Finish lake, where the two species have co-occurred for over 30 years. They found that P. leniusculus grow faster and that females reproduce for the first time at an earlier age than A. astacus. When co-occurring, P. leniusculus has a larger body size and larger chelae than A. astacus at the same age, which makes P. leniusculus superior in competition for food and shelter (Westman et al. 2002). Between 1970 and 1999 there was a change in the abundance of the two species in Lake Slickolampi (figure 8). A. astacus was the most abundant species in the 70s but P. leniusculus is the dominant species in the 90s (Westman and Savolainen 2001). Figure 8. Changes in relative abundance of Astacus astacus and Pacifastacus leniusculus in Slickolampi in 1970-1999. From Westman and Savolainen (2001). 31 Other introduced crayfish species have also been shown to be able to affect other species in the system they are introduced into. In northern Wisconsin lakes the introduced Orconectes rusticus greatly reduced macrophyte and snail abundance (Lodge and Lorman 1987). In the same study it was shown that O. rusticus was very effective in reducing single-stemmed macrophytes and by just one snip remove entire plants. P. leniusculus juveniles have been shown in experiments to dominate in competition with A. astacus juveniles for shelter, and juvenile A. astacus are thus more subjected to predation than P. leniusculus juveniles (Skurdal and Taugbøl 2002). Predatory fish strongly affect crayfish activity, aggressive behaviour and shelter use (Mather and Stein 1993), which lead to more competitive encounters between cooccurring crayfish species. This is happening in an Ohio stream where Orconectes saborni is almost totally replaced by the introduced Orconectes rusticus (Mather and Stein 1993). Hill and Lodge (1999) showed that O. rusticus strongly reduced growth in O. virilis when competing for food and that O. propinquus had an increased mortality due to competition and predation by O. rusticus. It has also been shown that individuals of successful invaders are able to use a broader range of information concerning predatory risk than native species (Hazlett et al. 2003). P. leniusculus has been introduced in Japan and there it have had a negative affect on native crayfish species, due to its larger size, more aggressive behaviour and better competitor for shelter and limiting resources than the native species (Nakata and Goshima 2003). As P. leniusculus seems to be superior to A. astacus this might lead to exclusion of A. astacus in Swedish lakes and streams where they co-occur. P. leniusculus has also been shown to consume more macrophytes than A. astacus in pool experiments (Nyström and Strand 1996, Nyström et al. 1999), which indicates that P. leniusculus may have a stronger effect on the benthic food web than A. astacus. One can argue that signal crayfish (P. leniusculus) will have a different effect on the benthic community and the energy flow in the food web than noble crayfish (A. astacus). There is evidence for a more aggressive behaviour (Vorburger and Ribi1999) and higher consumption that will structure the benthic invertebrate community both directly and indirectly. If the signal crayfish has a stronger impact on the ecosystem than noble crayfish is still not clear and further investigations on how the two species affect energy flow, the whole food chain and structure of communities are needed. 32 4. Proposed research The aim of my work is to assess the importance of predation and resource availability, on crayfish behaviour and abundance in lakes and streams. Another aim is to assess how cannibalistic crayfish really are and under what circumstances their cannibalistic behaviour is significant. During the whole work the differences between noble- and signal crayfish will be assessed. 4.1 Field study 1 Both abiotic and biotic factors affect the growth and abundance of crayfish. But which factor is most important and is it the same factor that controls growth and abundance for both nobleand signal crayfish? In several lakes with noble crayfish a field study will be conducted in august 2005. The lakes will differ in trophic status indicated by total phosphorus concentrations and by Secchi depths. Crayfish populations will be monitored using baited traps that will give relative estimate of abundance of larger crayfish (>6 cm total length). Fish populations (e.g. predators) will be monitored using benthic multi-mesh gillnets. All of the crayfish and fish captured will be measured for length and weight, and some will be sacrificed for analysis of gut contents and stable isotopes. Water samples will be taken for chemical analysis and physical parameters such as substrate size, depth and lake area will be determined at each site. A similar study has already been conducted in lakes with signal crayfish and my study will make it possible to do a comparison between the two species in terms of growth and abundance under different lake conditions in relation to substrate composition, trophic status and predator pressure. 4.2 Enclosure experiment Predation and competition are important structuring forces in food webs. How different predators and how the interaction (competition) among predators affect lower trophic levels are not very clear. A lot of studies have been conducted but often including only one predator or two interacting predators. In most natural freshwater systems a multiple predator effect is present and several predators interact with each other. How that affects the different predators and lower trophic levels has been less studied. 33 An enclosure experiment will be conducted in the summer of 2005 to assess how multiple predators affect each other’s foraging efficiency and lower trophic levels. In a stream where signal crayfish, trout and stone loach co-exist, 24 enclosures will be distributed in three groups (replicates) with 8 treatments in each. The enclosure set up can be seen in fig. 9 and the eight treatments can be seen in table 2. Ceramic tiles will be placed in each enclosure for measurements of periphyton growth for the different treatments. Table 2. The three predators and their presence (1) or absence (0) in the eight treatments. In all treatments invertebrates will be able to drift in and out of the enclosure and benthic invertebrates will be able to colonise the bottom of the enclosure. Signal crayfish Trout Stone loach Enclosure 1 (control) 0 0 0 Enclosure 2 1 0 0 Enclosure 3 0 1 0 Enclosure 4 0 0 1 Enclosure 5 0 1 1 Enclosure 6 1 0 1 Enclosure 7 1 1 0 Enclosure 8 1 1 1 Figure 9. An example of enclosure 2 where signal crayfish is present and the other predators are absent. Invertebrates are free to immigrate and emigrate. The enclosures will be left in the stream for one month and then the predators will be killed for further analyses. Gut content analysis will be conducted to se if the three predators have the same diet. Remaining invertebrates, detritus and algae in the enclosures will be collected 34 and measured to be able to compare the treatments effect on invertebrate, detritus and algae biomass. Drifting is an important escape mechanism in stream invertebrates and can be mediated by a predator. The drift in and out of the enclosures will be quantified by using driftnets both up- and downstream the enclosures to se how the different treatments affect drift behaviour in invertebrates. 4.3 Pool experiment 1, 2 and 3 Cannibalism is regarded as common among freshwater crayfish. If food is limited and there are high densities of crayfish they should eat their conspecifics according to previous studies. The lack of experiments and field studies makes me questioning this general idea. How cannibalistic are crayfish? Can predation indirectly affect cannibalism in crayfish through effects on crayfish behaviour? Is signal crayfish more cannibalistic, due to its more aggressive behaviour, than noble crayfish? To study the cannibalistic behaviour in crayfish, pool experiments will be conducted. One large adult crayfish (<10 cm TL) and 6 small (>4 cm TL) will be put in the same pool (four replicates) and then treated in three different ways (table 3). The experiments will be conducted with signal- or noble crayfish to test if they have different cannibalistic behaviours. If adult crayfish kills and eats the small crayfish it will be regarded as cannibalism, but if it is only the chelae that are lost and the small crayfish is not killed that will not be classified as cannibalism but noted. If a small crayfish attacks, kills and eat another small crayfish that will also be regarded as cannibalism. An example of the set up where fish will be present is shown in figure 10. Table 3. The three different treatments where the crayfish (1 adult and 6 small). How the different treatments affect the cannibalistic behaviour will be estimated by killed and eaten crayfish. Pool experiment 1. Food 2. Substrate 3. Fish Signal crayfish High quality Unsuitable With Signal crayfish Low quality Suitable Without Noble crayfish High quality Unsuitable With Noble crayfish Low quality Suitable Without 35 Figure 10. In the treatment with fish (perch) will be separated from the crayfish with a net so that perch are not able to eat the crayfish. How a predatory fish will affect the cannibalistic behaviour in both the large adult and in the small crayfish will be observed. 4.4 Field study 2 If the results from pool experiment 1,2, and 3 show that crayfish are cannibalistic another study will be conducted. First a pilot study will be done to see if it is possible to record crayfish in natural ponds. In a pond with high crayfish density, rather clear water and small area, four video cameras will be placed to monitor as much as possible of the pond bottom. The cameras will be left over night since crayfish are most active at night and then the films will be analysed to observe if any interactions between crayfish occur. If the pilot study works out well a larger study on several ponds with different crayfish densities will be carried out. 4.5 Time plan 04/05 05/06 06/07 07/08 Field study 1 Enclosure experiment Pool experiments Field study 2 Analysis Writing Courses, conferences 5. Acknowledgement I will thank my supervisors Per Nyström and Wilhelm Granéli for valuable comments on earlier versions of this manuscript. 36 6. References Abrahamsson, S.A.A. 1966. Dynamics of an isolated population of the crayfish Astacus astacus Linné. Oikos, Vol. 17, No. 1, pp 96-107. Abrahamsson, S.A.A. 1971. Density, growth and reproduction in populations of Astacus astacus and Pasifastacus leniusculus in an isolated pond. Oikos, Vol. 22, pp 373-380. Abrahamsson, S. 1983. Trappability, locomotion, and diel pattern of activity of the crayfish Astacus astacus and Pacifastacus leniusculus Dana. Freshwater Crayfish V, pp 239-254. Ackefors, H. and Török, K. 2002. 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En metodöversikt. Thomas Jonasson. 1975. Resistensbiologiska undersökningar över fritflugan (Oscinella frit L.) på havre. Jan Löfqvist. 1975. Bekämpning av skadeinsekter med doftlockning. Mats Carlsson. 1975. Synonymik, utbredning och ekologisk segregation hos knott (Diptera Simuliidae). En litteraturöversikt. Torbjörn von Schantz. 1976. Revirsystem och territoriellt beteende hos carnivorer. Torsten Dahlgren. 1976. Ekologiska synpunkter på stimbildning hos fiskar. Staffan Tamm. 1977. Why flock? A review of social behaviour in birds. Bo Ebenman. 1977. Födosöksstrategier hos fåglar. Allan Carlsson. 1977. Scandinavian passerine birds in their African winter-quarters. Fredrik Schlyter. 1978. Doftkommunikation hos barkborrar (Coleoptera, Scolytidae). Christer Löfstedt. 1979. Sexualferomoner hos fjärilshonor - kemi, biologi och användning för populationskontroll Hakon Persson. 1979. Jaktuttagets roll i andfågelpopulationers dynamik i relation till andra mortalitetsfaktorer. Boel Jeppsson. 1979. Vandringar hos smågnagare. Mikael Sandell. 1980. Scent communication in mammals, especially the carnivores. Jens Dahlgren. 1980. Limiting factors to some game birds. Thomas Madsen. 1980. Spatial organization and seasonal movements in snakes. Christer Brönmark. 1981. Feeding ecology of freshwater gastropods. Sigfrid Lundberg. 1981. Evolution i komplexa system. Paul Eric Jönsson. 1981. Social organization and breeding ecology of Calidris sandpipers. Torsten Gunnarsson. 1981. The effect of heavy metals on soil organisms. Olle Anderbrant. 1981. Population dynamics and dispersal of bark beetles. Einar B. Olafsson. 1981. Life history theory and field evidence in marine invertebrates. Karin Lundberg. 1982. Social organization in Microchiroptera. Jan-Åke Nilsson. 1982. Social status, resource utilization and life-time reproductive success in birds Henrik Smith. 1982. Evolutionary and functional aspects of hoarding. Inge Hoffmeyer. 1982. Coexistence of Apodemus sylvaticus (L.) and A. flavicollis (Melch.) in south Sweden. Jens Rydell. 1982. Foraging strategies in insectivorous bats. Peter Sundin. 1983. Plant-microorganism chemical interactions in the rhizosphere. Anders Tunlid. 1983. Microbe-surface interactions. Bill Hansson. 1983. Feromoner som isolationsmekanismer mellan närstående insektarter - ett elektrofysiologiskt forskningsomrΔde. Per Andell. 1985. Breeding biology and mating systems in plovers (Charadriinae). Roland Sandberg. 1985. Bird orientation: the relative importance of celestial and geomagnetic cues during ontogeny and migration. Kjell Andersson. 1985. Reproduction in aquatic insects. Inger Fröberg. 1985. Conflicts between the sexes in birds and mammals. Ann Erlandsson. 1985. Social interactions in semiaquatic bugs (Hemiptera, Gerromorpha). Anders Thurén. 1986. Effekter av ftalater I akvatiska ekosystem Mats Grahn. 1986. Cooperative breeding and demography in birds and mammals. Anders Helgée. 1986. Evolution of mating systems in precocial birds. Håkan Wittzell. 1986. Intersexual selection and mate quality. Åke Lindström. 1986. Fat deposition in migrating birds. Peter Anderson. 1986. Oviposition-deterring pheromones in insects. Katarina Hedlund. 1987. Fungivore - fungal interactions. Johan Nelson. 1987. Social organization in voles. Per Woin. 1988. Effects of pollutants on animal populations, communities, and ecosystems - An ecotoxicological research field. 43 49 50 Gudmundur Gudmundsson. 1988. Intraspecific variation in bird migration patterns. Roland Lindqvist. 1988. Microbial habitat specializations in oligotrophic ground waters. Papers listed below are divided into different sections within the Department of Ecology: A=Animal Ecology, E= Chemical Ecology/ Ecotoxicology, M= Microbial Ecology, L= Limnology and T= Theoretical Ecology. 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 Io Skogsmyr. 1988 (T). The interface between pollination, epidemilogy and chemical defence. Olof Regnell. 1988 (E). Origin and chemical speciation of mercury in freshwater environments with implicat ions for the uptake of mercury in fish. Staffan Bensch. 1989 (A). The significance of territory quality and male parental care in the evolution of polygyny in altricial birds. Mariano Cuadrado Gutiérrez. 1989 (A). Techniques of prey capture and foraging behaviour in arborealinsectivorous birds. Magnus Augner. 1989 (T). Game theory in ecology. Dennis Hasselquist. 1990 (A). Bird song and sexual selection. Lena Tranvik. 1990 (A). Adaptations to changing environments; applications in the study of soil fauna Almut Gerhardt. 1990 (E). Effects of heavy metals, especially Cd, on freshwater invertebrates with special emphasis on acid conditions. Susanne Åkesson. 1990 (A). Animal orientation in relation to the geomagnetic field. Noél Holmgren. 1990 (T). Density dependent spatial distribution of individuals. Maria Sjögren. 1991 (A). Patterns in dispersal with special reference to soil collembola. Jep Agrell. 1991 (A). Infanticide in rodents. Anders Hedenström. 1991 (T). Optimization of migration performance in vertebrate swimmers, flyers and runners. Mats Svensson. 1991 (A). Mate choice in moths K. Ingemar Jönsson. 1991 (T). The cost of reproduction hypothesis. Peter Nilsson. 1991 (A). Soil structure and earthworms: Interactions and disturbances. Håkan Ljungberg. 1991 (A). Pheromone perception in male moths - functional morphology of the olfactory system. Pär Ingvarsson. 1991. (T). The effects of vector-borne fungal pathogens on natural plant populations. Mia Ramgren. 1992. (E). Surface behaviour of bacteria in oligotrophic ground waters. Ulf Ottosson. 1992. (A). Parent-offspring conflict, sibling competition and the evolution of begging in birds. Ola Olsson. 1992. (A). How to exploit a patchy variable environment? Zhu Junwei. 1992. (A). The evolutionary interpretation of variation in moth sex pheromones phylogenetic aspects. Cecilia Järnmark. 1992. (E). Loading of organochlorines to a waterbody; Fate within the Baltic Sea. Göran Ewald. 1992. (E). Toxic persistent organic compounds in sediments. Erik Svensson. 1993. (A). Energetic constraints and reproductive tactics in birds and mammals. Peter Valeur. 1993 (A). Mate-finding in insects; Signal/Response roles and associated costs. Lars Pettersson. 1993 (A). Foraging under risk of predation: trade-offs and indirect effects in aquatic habitats. Wu Wenqi. 1993 (A). Moth sex pheromone communication - mechanisms of specificity in production and response. Nils Kjellén. 1993 (A). Moult in relation to migration in birds. Patric Nilsson. 1993 (T). On the ecological and evolutionary significance of bud and seed dormancy. Maria Sandell. 1993 (A). Intra-sexual competition among females Irene Persson. 1994 (A). Influence of nest predation on clutch size Johannes Järemo. 1994 (T). The plant as an economic institution. Christer Bergwall. 1994 (E). Acclimatization and adaptation to changes in the environment: a microbial perspective. Ulf Wiktander. 1995 (A). Territory quality in altricial birds. Samuel A. Ochieng. 1995 (A). Primary olfactory centres in invertebrates and vertebrates. Olof Berglund. 1995 (E).The effect of lake on uptake of pollutant by zooplancton. Anders Nilsson. 1995 (A). Habitat complexity and the influence on predators and prey, and their interactions. 44 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 Darius Sabaliunas. 1995 (E). Semipermeable membranes and passive partitioning approach in environnmental analysis. Åsa Langefors. 1995 (A). Ecological aspects of genetic variation in Salmonin fishes. Thomas Ohlsson. 1996 (A). Sexual signals and parasite loads. Björn Lardner. 1996 (A). Effects of competition, desiccation and predation on performance and metamorphosis of Anuran larvae. Cecilia Backe. 1996 (E). Atmospheric transport and uptake of persistent organic compounds in terrestrial ecosystems. Ralph Tramontano. 1996 (A). Dispersal and migration in terrestrial amphibian populations. Anna Wallstedt. 1996 (E). Allelopathy in plant-plant interactions. Anders Å. Karlsson. 1996 (E). Phospholipids, Spingomyelins and other polar lipids - analysis of structural and physiologically active lipids by liquid chromato- graphy-mass spectrometry. Roger Härdling. 1996 (T). The logic of evolutionary conflicts. Liv Wennerberg.1997 (A). Genetic variation between bird populations. Mario Pineda. 1997 (T). The ghost in the closet of evolution. Helena Westerdahl. 1997 (A). The variability of MHC genes in vertebrate populations. Anders Kvist. 1997 (A). Energetics of bird migration. Anna-Karin Augustsson. 1997 (A).How on earth do they do it in the soil? Modes of reproduction of the soil invertebrate fauna. Ruey-Jane Fan. 1997 (A). Experimental studies of learning capacity in insects. Rickard Ignell. 1997 (A). Locust phase polymorphism: Pheromonal and hormonal influence. Fredrik Östrand. 1998 (A). Monitoring insects with traps; functions and problems. Mattias Larsson. 1998 (A). Neural integration of olfactory information in insects. Bengt Hansson. 1998 (A). Selection against inbreeding and outbreeding: the evolution of optimal outcrossing. David Abraham. 1999 (E). Phylogenetic methods for inferring the evolutionary history and processes of change in ecological-, morphological- and molecular- characters. Glenn Svensson. 1999 (E). Mating disruption in moth. Genetic, behavioural and electro physiological aspects. Camilla Ryne. 1999 (E). The function of pheromones and their use in IPM of stored product moths and beetles. Lars Råberg. 1999 (A). Natural selection on condition-dependent traits. Maja Lindeblad. 1999 (M). Morphogenesis of nematode-trapping fungi. Mikael Rosén. 1999 (A). Experimental approaches for studying vertebrate flight in a wind tunnel. Johan Bäckman. 1999 (A). The ontogenetic development of compasses in migratory birds. Jonas Hedin. 1999 (A). Insect dispersal in relation to habitat predictability in nemoral and hemiboreal forest. Dagmar Gormsen. 2000 (A). Indirect ecological interactions: consequences for ecosystem functioning and importance for soil processes. Dainius Plepys. 2000 (E). Odour mediated interactions between insects and plants. Antoine Le Quéré. 2000 (M). Molecular events during ectomycorrhiza development. Mikael Carlsson. 2000 (E). Mixture interactions - non-linear processing of complex odours. Arnout ter Schure. 2000 (E). Describing the Flows of Synthetic Musks and Brominated Flame Retardants in the Environment: A New Ecotoxicological Problem? Maria Hansson. 2000 (A). The Biotransformation System; - Ecological, Evolutionary and Genetic Perspectives Jakob Lohm. 2000 (A). Evolution and maintenance of MHC variation. Jonas Nilsson. 2000 (A). Predation, a generality in marine habitats Martin Green. 2000 (A). Flight directions of migrating birds in relation to wind. - The question of drift or compensation Samuel Kiboi. 2001 (T). Sexual selection and mate choice: The female’s perspective and role in geneflow. Margaret Nkya. 2001 (T). The effect of different environmental factors on gene transfer through pollen dispersal. Teklehaimanot Haileselassie. 2001 (T). The Effect of Environmental Factors on Male and Female Reproductive Functions. Rachel Muheim. 2001 (A). Animal Magnetoreception - Models, Physiology and Behaviour. Patrik Karlsson. 2001 (T). Food webs and Extinction. Christian Olsson. 2001 (E). The function of food volatiles: Insect behaviour and pest control. Richard Ottvall. 2002. (A). Nest predation in waders: A landscape perspective 45 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 Niklas Holmqvist. 2002. (E). The Influence of Trophic Status and Habitat Utilization on Pollutant Uptake in Benthic Foodwebs. Helene Bracht Jρrgensen. 2002. (A).Dietary self-selction in insects: behaviours and mechanisms. Anna Gårdmark. 2002. (T). Life-history evolution in harvested populations: Theory and the lack of it. Helen Ivarsson. 2002. (T). Hypobiotic life stages. Peter Frodin. 2002. (T). Community dynamics. Ken Lundborg. 2002. (T). Speculations on the avian hippocampus, spatial memory, and the costs thereof.. Germund Silvegren. 2003. (E).Circadian clock mechanisms regulating sex pheromone communication in moths. Oskar Brattström. 2003. (A). The orientation mechanisms and migratory patterns in day flying Lepidopterans. Maria Persson. 2003. (E). The threat to the Baltic salmon - A combination of persistent pollutants, parasites and oxidative stress. Christin Säwström. 2003. (L). Viral dynamics in the microbial loop. Johanna Stadmark. 2003. (L). What regulates the emission of greenhouse gases from wetlands? Marika Stenberg. 2003. (L). Can animals behave optimally in social foraging situations? Kelly C. Gutseit. 2003. (L). The Role of Planktonic Ciliates in Lakes with Different DOC Content. Anna Nilsson. 2003 (A). Partial migration - contrasting theories Måns Bruun. 2003. (A). Mechanisms limiting breeding birds associated with farmland Lina Kristoffersen. 2003. (E). The chemical ecology of Homoptera - from host plants to conspecific interactions. Martin Stjernman. 2003. (A).The evolution of virulence: an introduction to some models Sara Henningsson. 2003. (A). Factors determining the geographical ranges of species. Pia Hertonsson. 2003. (L).Can winter migrating cyprinids cause a shift between alternative stable states? Martin Granbom. 2003. (A). Long-term effects of early growth conditions in birds. Ullrika Sahlin. 2003. (E). Risk analysis of alien species. Lena Månsson. 2003.( T). How to detect the drivers of large herbivore dynamics. Erik Öckinger. 2004. (A). Extinction in heterogeneous landscapes - effects of stochastic and deterministic processes on the persistence of insect populations in fragmented areas. Jacob Johansson. 2004. (T). Models of ecological communities and their predictions on diversity and stability. Jessica Abbott. 2004. (A). Conflicting selection pressures. Francisco Picado. 2004. (E).Mercury in the environment and the gold mining activity in the St Domingo district, Chontales-Nicaragua. Mikael Åkesson. 2004. (A). Quantitative traits and QTL. The next approach to explain the phenotypic variability in natural populations. Marta Nilsson. 2004. (T). Intermittent locomotion in water, air and on land. Olof Hellgren. 2004. (A). A parasite persspective of malaria vectors - Obstacles, life history trade-offs and manipulations. Emma Ådahl. 2004. (T). Population responses to environmental influence. Ramiro Logares. 2004. (L).Biodiversity, biogeography and molecular ecology of freshwater dinoflagellates. Katia Montenegro Rayo. 2004. (E). Ecotoxicological effects of DDT and glyphosate on aquatic organisms: a case study Karin Olsson. 2005. (L).The importance of predation, cannibalism and resources for production and abundance of crayfish. SE-LUNBDS/NBLI-05/5007+42pp ISSN 1100-1844 46
