Whilst studying at the University of Plymouth an integral part of my degree consisted of an honours project. Within the grounds of the university is a small reservoir that holds stocks of crucian and common carp, this gave me the perfect opportunity to examine an area of freshwater biology close to my heart. The aim of the research was to investigate the feeding interactions among species within the reservoir. This page aims to outline the main findings and conclusions of my research. The project is posted and key areas and points of interest can be quickly located in the abstract and conclusions. Due to the difficulty of reading a 10000 word thesis on a single web page the full manuscript is available on e-mail request. I hope you enjoy the findings of my project and I would be grateful of any constructive feedback.
The food choice of crucian carp (Carassius carassius) in Drakes reservoir and the influences upon on this by the aquatic environment were investigated.
Thirty-five fish stomachs were observed and it was found that the feeding preference of the crucians revolved around chironomid larvae (Chironomus), small bodied pelagic cladocera (C. ovalis), benthic cladocera (A. affinis) and one species of ostracoda (Cypridopsis). The chironomid larvae and benthic cladocera became more important as the fish increased in length. Rotifers and phytoplankton were not an important part of the diet; Arcella were utilised, but in unknown proportions.
It is suggested that heavy macrophyte growth was the main organism responsible for many interactions and influences upon the fishes' diet and species diversity in the reservoir.
This population of crucian carp is omnivorous, relying upon more benthic organisms as they increase in length. Stunted growth suggests that intraspecific competition is prevalent in the reservoir. Interspecific competition with common carp (Cyprinus carpio) is suggested. It is believed the crucian carp have reverted to a more cladoceran-based diet to combat this competition with the common carp; this indicates a predominately benthic niche overlap between species.
The study of interactions between the links in complex food chains can lead to an understanding of how specific organisms gain their food sources. Many components constitute these intricate food chains, from the smallest bacteria, to the largest fish species; these all have consequential roles when assessing the ecological stability of a body of water. To advance the knowledge of feeding preferences of any one particular species, an understanding of the broader aquatic community is a requisite.
In freshwater fisheries management and aquaculture, the evaluation of natural food biomass is of importance, as in many cases, this is the primary source of food; sometimes the addition of artificial feeds are used as supplements. To gain an equilibrium between the feeding of natural and artificial food, careful monitoring must be undertaken; this is essential due to the variability created by natural conditions. Just as significant is gaining an idea of the most utilised, most easiest obtainable and highest calorific value organisms as these all aid the development and growth rate of the species further up the food chain.
This study is aimed at producing a representation of the main elements of the food chain within Drakes Reservoir, culminating at the pinnacle level, the crucian carp (Carassius carassius). This fish species is quite unique (Penttinen & Holopainen 1992) as it has an option of not feeding throughout the winter sometimes for a period of 6 months; this is achieved by storing large amounts of glycogen within the liver (Hyvarinen et al. 1985). The crucian carp also has the ability to morphological deepen its body as predator avoidance (Brönmark & Miner 1992) usually resulting in low stocking densities. Without the presence of predators they commonly allow themselves to over populate and stunt in small ponds (Holopainen & Pitkanen 1985).
The crucian carp is not commonly seen for sale as a food fish in the United Kingdom, however world production stood at approximately 862,000 tonnes in 1997, this was an increase of nearly 720,000 tonnes since 1988 (Anon. 1999). These figures indicate that this species is increasing in popularity therefore any study regarding its feeding habits may help producers understand the importance of natural food within culture operations.
Due to the apparent abundance of crucian carp accumulated within Drakes reservoir the following hypothesis has been proposed. The species will utilise the most available and most prominent organisms within their habitat. To achieve this the following questions will be addressed:
1) Are there any important interactions between aquatic organisms that may influence the food choice of crucian carp?
2) Does the diet in sampled fish, in terms of specific organisms, vary to any great extent and is it influenced by intraspecific competition?
3) Would the influence of larger, more vigorously feeding fish species, affect the chosen feeding patterns in terms of inter-niche competition?
1.1 The role of niches in a water body containing fish
Weatherley (1963) considers the role of niches among freshwater fish and their connection to the food chain. This could prove important as the site of research also contains common carp (Cyprinus carpio). In the authors experience this species is a more aggressive feeder than the crucian carp, therefore if a similar, if not identical food source is required by both the crucians may end up being pushed onto an energetically inferior food as a result of intense competition.
The closer that different species rely upon the same food source, increased competition will result (Werner et al. 1977). Weatherley (1963) describes the role of an animal in its ecosystem by referring to its 'niche'. If two species are found to share the same niche, or even have an overlap, the weaker will certainly languish. Hanson & Leggett (1986) gave evidence of this situation with a study comparing the pumpkinseed (Lepomis gibbosus) and yellow perch (Perca flavescens). Their results demonstrated that the perch adjusted its feeding habit from <1% to 30-53% of microcrustaceans in total diet composition. This modification was induced by the introduction of the pumpkinseed, a superior competitor; importantly, the micro-crustaceans were an energetically inferior food, consequently the perch were to suffer.
Shifts in food source can also be due to immediate risks of direct predation upon themselves (Paszkowski et al. 1996). Additionally, these changes can lead to indirect mortality due to reductions in quality and quantity of food in the total diet; this may be a result of predator avoidance (Werner et al. 1983). There are situations of harmonic multi-species communities where certain members have a wide enough food spectrum to avoid the threat of competition (Persson 1987).
Niches comprise many components of a food web, some of which will be impracticable to detect under standard laboratory conditions. Many published food webs disregard the predation and consumption of minor species (Pimm et al 1991) and without additional, more profound studies, these elements will also remain absent from this investigation. It is expected that various organisms will be discovered whilst undertaking this study with the majority playing important roles in the preferred feeding habits of the crucian carp.
1.2 Review of the organisms present in a freshwater environment
1.2.1 Bacteria and small phytoplankton
Although bacteria are the smallest organism present, they are an important element in the aquatic food web. Stevenson et al (1996) notes the importance of the link between excreted photosynthetic products of algae and the utilisation of these by bacteria. Beveridge et al (1991) suggested that small carp had the capability to ingest unattached bacteria and Matena et al (1995) employed fluorescent labelling to gain evidence of this. Therefore, the role of bacteria in the feeding of carp cannot be underestimated as this literature demonstrates.
Another theory on the role of bacteria and fish links mixotrophs, organisms that feed and photosynthesise; this allows a less energetic way for larger fish species to ingest quantities of bacteria. No specific literature associating the theory of phagotrophic protozoans to freshwater has been ascertained, but Stoecker (1992) and Sheer & Sheer (1991) deliberate its occurrence in oceans. It could be a possibility that this process occurs within freshwater bodies, but research is required in this area before scientists can be certain.
The transformation of ultra-fine organic matter, mainly bacteria, into an accessible particle size for crustacean zooplankton to utilise takes place through ciliate protozoan microzooplankton. Porter et al (1979) gives evidence that both Daphnia and Cyclops, important food sources for the carp, feed on these ciliate protozoans, thus fashioning another important food chain link between bacteria and carp. Generally bacteria are fundamental to the environment as they assist the breakdown of dead plant material and animals. The majority are unicellular and range from 1-50µm (Maitland 1990). It is unlikely they will figure in this study due to size, but this evidence suggests they are too important to disregard.
The higher the trophic level the more importance the organism has to the adult carp. The stage succeeding bacteria incorporates the green algae and although not of categorical importance to the older year classes the young larvae are habitually dependent on these planktonic organisms (Gerking 1994). Various species occur in freshwater from non-motile unicells and colonies, swimming colonies to non-motile unicellular and filamentous green algae. They vary in size from 1mm to trailing forms that achieve over 1m in length (Belcher & Swale 1978).
Particular species of herbivorous fish depend solely on algae, but the carp, generally referred to as an omnivorous bottom feeding species (Crivelli 1981), tend to utilise more than just algal forms. Appler & Jauncey (1983) have explored the role of filamentous algae in conjunction with aquaculture and results showed potential for using the protein content as a part diet for tilapia (Sarotherodon niloticus).
Protozoa, ciliate and flagellate, are prevalent in most standing waters and as previously mentioned they support links throughout the food chain. No literature has been encountered implicating these directly as a principal food source of carp; findings from the present experimental gut analysis may help to clarify this.
1.2.2 Zooplanktonic crustaceans
The zooplanktonic crustaceans, copepod and cladocera, are proven to be significant natural food sources of carp resulting in many scientific investigations involving these organisms. Ogino (1963) calculated that Daphnia species contained upwards of 60% protein levels while Vijverberg & Frank (1976) detected that Daphnia contained nearer to 69% of total organic matter with Cyclops exceeding that figure by an additional 2%. This study appears fairly unique as it aggregates calculations of carbohydrate, lipid, and total nitrogen levels in conjunction with protein. Many other papers single out one aim; for example Dabrowski & Rusiecki's (1983) study of free amino acids in zooplanktonic food (copepods) of fish larvae.
The nutritional energy values of aquatic invertebrates were investigated by Salonen et al (1976) and their calculations were made with a relationship to organic carbon content due to their views of the inaccuracy of equivalent results given in ash-free dry weight (Ogino 1963, Vijverberg & Frank 1976). This trophic level has more research with regard to natural food sources in fisheries and aquaculture than any other. Although this study will only entail uncomplicated observations from resultant gut analysis the importance of this group should be recognised, as it may constitute a significant component of the results.
Mentioned previously have been aspects of competition among species sharing trophic levels, but as with numerous life forms, the prey has a tendency to contest predation by various means.
Cladocerans are one of the most important species of zooplankton available to the carp and it seems relevant to introduce their attempted resistance to predation at this point. Vanni (1987) highlighted that fish predation affected the life history traits and size structure of cladoceran communities; pools without fish revealed the tendency of growth to larger sizes. When fish were present, threat of predation compelled cladocerans into earlier maturity and production of smaller young, hence reducing their exposure to size-selective predators. Archibald (1975) observed higher levels of fecundity when in the presence of fish and Lynch (1979) showed that daphnia populations increase when lower order plankton are being preyed upon, although this increase did tend to cause interest from alternative predators.
These are a few examples of how heavily predated species can combat threats to their community, but the carp, a species able to utilise a manifold of organisms, would seldom be effected by the loss of just one food source.
Further species involved in freshwater food webs include rotifers (important to the younger year classes), molluscs, malacostracans, branchiopods, aquatic insect larvae, small water bugs, and aquatic beetles. Many of the larger species may not emerge in laboratory experiments due to the difficulty of consumption by smaller sized fish.
1.3 Prey-predator relationships and the benthic community
Studies into prey-predator relationships are prevalent and with the economic importance of producing artificial fish diets used in conjunction with available natural food sources the world of aquaculture is no exception. Using rotifers as a food source, Khadka & Ramakrishna (1986) observed that carp were taking prey to a length of 1570µm by the age of 30 days. Hason & Macintosh (1992) demonstrated that similar sized carp preferred food particle sizes of 0.2-0.4 that of their mouth size. These findings suggest that the majority of previously discussed organisms will surface in the subsequent experiments with only the largest insects remaining absent.
Discussion so far has aimed to describe the aquatic environment with assistance of additional writers' work. A simplistic panorama of the aquatic community has been outlined, but in reality this community is divided into many complex areas. The aim of this study is to gain an insight into the feeding preferences of one species, but for clear results an understanding of where the aquatic organisms can be found is required. As the carp is recognised to feed on pelagic and demersal species, investigational studies of these areas is imperative.
Although the freshwater planktonic community is extensive some of the larger organisms, more importantly insect larvae and molluscs, can be discovered predominately in the benthos. The benthic community and its interactions with fish are a widely researched area due to its importance in the stability of a water body. Batzer (1998) discovered that carp severely reduced densities of benthic midge larvae in early July and by late August, when the carp had reverted to alternative food sources, the midge community failed to recover due to unsuitable breeding conditions. This demonstrated a variation in food web structure created by prey-predator relationships. Brönmark (1992) obtained similar results with studies of interactions between pumpkinseeds and snails. He found that predation of the snail by the pumpkinseed increased the periphyton (Filamentous blue-green and colonial green algae) biomass thus an alteration in the food web. The same results were apparent from Brönmark's (1994) study of tench (Tinca tinca) and freshwater snails and their resultant effects upon the benthic food chain.
Diehl's (1992) investigation into the interaction between fish species, in this case the perch, and the benthic community and Death's (1995) attempt to explain habitat stability in benthic invertebrates give indications of the importance of this area in the eco-system. Spataru et al (1980) observed the connections between benthos, carp and supplementary feeding and concluded a preference for zoobenthos under natural conditions reverting to higher water column zooplankton, mostly copepods, as a result of the demand feeding. The important point is the utilisation of various levels of the water column when required.
1.4 The influence of macrophyte - Elodea canadensis
The field site is densely abundant with Elodea canadensis, a submerged, semi-rooted, aquatic pondweed. Weed in this quantity may have influences upon available sources of food; it is able to support a varying array of aquatic life; it will create competition with forms of filamentous green algae; it is possible that the plant will be nutritious enough to supplement the fishes diet.
The competition aspect is again intriguing, as ponds with large quantities of submerged weeds tend to dictate some orders of the food chain. An interesting study showed that the daphnia species were dissipated in heavily weeded ponds due to the deficiency of larger green filamentous algae, their main food source (Irvine et al 1989). The available space was then filled by an increase in smaller cladocera species (Simocephalus), these tending to feed on small diatoms.
The role of physical and chemical factors and their significance to this study require brief discussion as many aquatic invertebrates are dependent upon temperature, light, water quality and various other factors. These are important daily and seasonal influences and must be considered when conducting sampling; this investigation will be conducted over a short time span thus water quality will not be as important as light or temperature. For more accuracy, an experiment of this nature should be conducted over a period of months thus giving a clearer perspective of possible natural influences and predator-prey relationships. This of course is just a simple investigation but it should be noted that the site utilised in this experiment has the scope for larger, more investigative long-term studies in the field of fisheries science.
1.5 Review of stomach content analysis techniques
The basis of this experiment involves the investigation into the content of the crucian carp's stomach; this is a common and useful way of analysing the food web of a marine biological community (Berg 1979).
Various techniques are available to scientists when undertaking the gut analysis of fish. The selection of an appropriate technique will ultimately be determined by the investigation type, presented hypothesis, or nature of the food to be analysed (Windell & Bowen 1978); although on occasions the equipment, time scale or site restriction may take precedence. The following paragraphs will briefly review the most commonly applied techniques.
The simplest available method takes organism occurrence as the main consideration. Recording the number of stomachs containing one or more specific food category can be graphically represented as the percentage of stomachs containing each organism or group (Hyslop 1980). This method is expeditious and only requires the minimal of apparatus, but seldom gives evidence of accurate quantities or preferences regarding each food category present. In relation to previously discussed environmental influences this technique is ideal for portraying seasonal changes in diet composition (Frost 1977).
Numerical methods can be applied by enumerating the individuals in specific categories; this is undertaken for all stomachs, the sum is expressed as a percentage of total individuals in all food classifications (Crisp et al. 1978). This application is relatively fast and simple; this will be influenced by the feasibility of prey item identification. Methods of sub-sampling may be performed to eradicate the tiresome nature of very diminutive organisms. With a view to statistical analysis this technique allows the computation of the mean organisms in each stomach. As with any method hindrances will be apparent; inaccuracies when dealing with detritus and microalgae; overemphasis of importance regarding small prey items (Crisp et al. 1978). Crucially, Hyslop (1980) notes that number of organisms in a carp stomach are difficult to appraise due to mastication of food items before they reach the area of examination.
Gravimetric methods are frequently applied when ascertaining calorific intakes of fish; this method allows weight of food to be determined wet or dry. Finally, methods of extracting stomach contents can be employed if the killing of fish endangers the population or if only odd large fish are being sampled (Petridis & O'Hara 1988); this is generally impractical for small species.
2.0.1 Site description
The field site is a disused concrete reservoir adjacent to the grounds of Plymouth University, Devon. Due to reduced water levels the reservoir is commonly divided into two distinct equally sized unattached sections. Water depths are almost constant within sections and range from approximately 2 metres tapering to 0.75 metres intersection; shallowing appears to be a consequence of heavy silting. There is a drop of approximately 4.5 metres to the centre partition; this was accessed by the use of a ladder. Samples were gathered during the period 12th September to 30th October 1999 using various collection procedures.
The collection of fish samples was restricted due to the difficulty of accessing the waters edge. Seine and gill netting methods were not feasible due to heavy weed growth throughout the reservoir; unwanted bycatch was also a problem. Alternatively, samples were collected by the use of simple angling techniques; rod and line utilising barbless hooks.
2.0.2 Fish capture techniques
Angling depth required consideration as an incorrect selection would encourage the capture of unwanted species. Single baits without the addition of extra particle feeding was utilised so not to disrupt daily feeding patterns of the fish. Maggots were an ideal bait as the large size and easy identification would aid seperation if consumed into the stomach. It was felt that unnecessary particles of feed would instigate heavy foraging resulting in food items not normally consumed under natural conditions, appearing in later dissections.
All fish captured were measured then weighed on accurate digital scales, body cavities were opened and entire stomach contents were removed, labelled and stored in glass jars under freezing conditions.
2.0.3 Laboratory techniques
General observations were made with a zoom stereo microscope, range 0.7-4.5, x20 wide-field eyepieces and x2 extra objective lenses giving total magnification of x180. Gut contents were studied scrupulously and notes made on organisms present. The contents were observed in sub-samples; as a whole stomach the quantity of material impeded adequate viewing. Each sample was combined with clean tap water and broken down cautiously to reveal whole, identifiable organisms. The frequency of occurrence method (Bowen 1983) was applied which enabled the production of suitable graphs representing percentage of stomachs against length of fish.
Two techniques were available for obtaining images of prevalent organisms. Firstly, the utilisation of photographic equipment coupled to a compound microscope presented perceptible images of the diminutive individuals. This system comprised of an Olympus OM-2 camera with a 5052 Tmx Kodak black and white film. The camera was attached to the compound Olympus BH microscope via a 'C' adapter with differential interference contrast; magnification was utilised to x120. The resultant films were developed by photographic media services, University of Plymouth. This method required the preparation of standard glass slides with cover slips; no fixing chemical was used.
The second method applied to gain images required the use of a scanning electron microscope; this process was very lengthy and somewhat unrewarding. Once removed from the stomach the sample of organisms was placed in a fixing chemical, 25% Glutaraldehyde, for approximately one hour. Once fixed the chemical was removed with a glass pipette and varying ranges of ethanol was added to dehydrate the sample; range included 30%, 50%, 70%, 90% and two lots of absolute. Each range was left to stand for approximately 5-minute durations; this process was conducted within a fume cupboard.
Once fully dehydrated the remaining liquid ethanol was removed with a critical point drier, the sample then placed upon a conductive metal stub, placed into a splutter coater and duly coated with gold; this allows the electrons to conduct within the microscope. The finished sample was then placed into a JSM-6100 scanning electron microscope where images were created. Difficulties with organism destruction did arise with this method, but the superior quality of the images can be fully realised within the result section.
2.0.4 Fish independent sampling techniques
To ascertain where identified organisms reside within the reservoir further biological sampling was a necessity. Water samples were gathered by deploying submerged bottles from the partition wall access. A small bucket fastened to a lengthy rope was also used to gain indiscriminate samples from the reservoir's deeper, less accessible areas. These methods enable indications of smaller phytoplankton normally unattainable with alternative collection techniques.
Water column samples were gained by towing a plankton net, cod end mesh size 200µm, through mid-water. With the reservoir being split by a low partition the net was lowered safely into the water, then with slow dragging motions, towered to the opposite side, a distance of approximately 30 metres. Only two suitable openings were available on the left side and just one on the right. This technique collected the mid-water zooplankton and the largest pyhtoplankton
Benthic samples were collected via the use of a long hollow pipe, 3cm in diameter and 1.5 m in length. This tool was lowered to approximately 2 cm above the reservoir bed with the exposed end covered and then once in position, uncovering allowed air to be released creating a suction effect; the result was benthic material being drawn into the tube. The end was then re-covered and the pipe removed, materials were then discharged into a container. The accuracy of this method was unknown, therefore results may be unreliable. It is hoped that the most prevalent larvae were accumulated with this method.
The collection of weed samples was undertaken with two simple techniques. Firstly, collections by hand from close to the partition wall and secondly with the assistance of a rake head connected to a rope; this enables alternative samples to be taken from the deeper areas. The severity of the rake method induced losses of important individuals when retrieving; hand collection seemed to lead to more precise results. Many organisms are prevalent in weeded areas hence the importance of these collections. Finally, by the use of a small knife samples were scrapped from the concrete sided reservoir walls.
Once collected the samples were transferred from their respective containers with a small long nosed pipette and placed on a series of petri dishes and glass slides. These were viewed underneath the same light microscopic equipment as previously discussed.
3.1 Length/weight relationship of crucian carp
Fork lengths of the crucian carp sampled were from 11.2 cm to 13.6 cm and respective weights correlated well with length as shown in Fig. 1 (R2 = 0.91). Some smaller crucians (<8cm) were caught and returned, but no larger specimens (>13.6cm) were obtained. Only 3 specimens (>13cm) had reached maturity, these contained ova but no mature males were observed. As expected some large common carp (>25cm, >500grms) were caught and returned immediately. Although only a small variation in the size of crucian carp was apparent, some marked differences in gut contents were observed.
3.2 Diet of crucian carp
A total of twenty organisms were identified within the stomachs of the carp. Organisms by name, total and percentage occurrence of stomachs can be seen in Table 1 with graphical representation in Fig. 2. Phytoplankton was present in all sizes of fish, but only in small quantities; a small increase was observed in smaller specimens (<12.1cm). Observed phytoplankton included Scenedesmus (Fig.12) and Pediastrum (Fig.9 and 10) with the former being the more prominent of the two. There was no visual relationship between percentage occurrence of stomachs and fork length. Overall the most prominent phytoplankton was a form of filamentous green algae (Fig.11); this occurred in every specimen with larger quantities prevalent in specimens <12.2 cm.
Diatoms were limited in variety with only Pinnularia being successfully identified. This diatom was present in 13 stomachs; no preference among certain sized specimens was apparent. One of the most prominent organisms identified was the protozoan Arcella. Identification of Arcella took place in 34 out of 35 fish stomachs examined and visual quantities were high. The water mite, Piona conglobata, appeared in only 10 stomachs with these being in very small quantities (mostly singular), all observations were made in the larger of the specimens.
| in larger specimens (>12.2cm) and Chaoborus appearing in a total of 5
of the larger fish stomachs. The occurrences in larger fish can be seen
clearly in Fig.4 with the obvious bias of observations to the right of the
The largest quantity of organisms observed belonged to the cladocerans group. Three main species of closely related pelagic cladocera were identified, with Chydorus ovalis (Fig.17) appearing in 100% of stomachs: Eurycercus lamellatus (Fig.19) in 89%: Sida crystallina (Fig.18) in 60%. The benthic cladocera Alona affinis (Fig.20) was observed in 60% of total stomachs.
The relationship between the occurrence of these four organisms and fork length can be seen in Fig. 5. Pelagic ostracoda, Cypridopsis (Fig.15 and 16) (97% of stomachs), and large pelagic cladoceran, Daphnia pulex (26%), were also observed. The occurrence of D.pulex can be seen in Fig.6 alongside the copepod, Cyclops (23%), and the Nauplii of Cyclops (19%). These all have low observed frequency but do occur in very distinct length groups.
Finally, detritus was observed in every stomach with the majority being
made from small pieces of macrophyte (Fig.7); no green macrophyte was
observed within any stomach. Other unusual sightings were made with the
most interesting being a section of damselfly nymph; this can be seen
in Fig.8. Figure 22 shows some unidentifiable material found within the
stomachs. Although most organisms were complete certain occasions arose
where no positive identification could be made.
| 3.3 Aquatic investigation
and food web construction
Unfortunately, the collection of data that would have enabled the construction of a food web was somewhat sparse. Due to difficulties with many of the sampling techniques an insufficient quantity of positive data was gathered to complete this task. This failure was not completely disastrous, some positive points have been gained linking certain organisms with their respective habitats.
Pelagic bottle samples showed the four species of rotifer identified in the stomach analysis, very little phytoplankton was discovered. The plankton net revealed small quantities of Cyclops and D. pulex in open water (the only accessible area). No other cladocera were uncovered with this technique although this may have been influenced by the respective cod end mesh size.
Samples of Elodea canadensis produced very little in the way of helpful information. Large organisms such as damselfly nymphs (Hyponeura) and various species of nematode worm were discovered, but no link with the stomach contents could be found (the large size was the important factor); Chironomus and Cypridopsis also appeared in small numbers.
The partition wall scrapings consisted mainly of blanket algae, but within this was found Cypridopsis and C. ovalis. Finally, the benthic samples gave indication of only one organism, Chironomus. The method applied when collecting benthic material was far harsher than expected thus giving samples from deep below the top layer. This led to a large quantity of material that contained very few identifiable organisms.
3.4 Photographic representation of some organisms present within the stomach
|3.4.2 Green and Filamentous algae|
Figure12: Scenedesmus (x550). Another commonly occurring
3.4.3 Rotifers and Ostracoda
4.1 Aquatic invertebrates and their interactions within the reservoir
The collected data is insufficient to construct a scientifically based aquatic food web, however, conspicuous interactions between the identified organisms can be distinguished. The subsequent paragraphs will outline the specific areas within the reservoir that these organisms were located and any interactions that may take place prior to predation by the fish species present.
4.1.1 The influence of macrophyte within small water bodies
Clearly the first discussion topic must focus upon the intense growth of Elodea canadensis observed within the reservoir. This macrophyte favours high levels of silt deposition for growth throughout the summer months and then supposedly dies down in winter (Preston & Croft 1997). A return visit to the field site in February clearly showed no reduction in macrophyte quantities and little discolouring of chloroplasts.
Silt accumulation upon the reservoir bed could be clearly seen at the deepest point, approximately 1.8m, thus showing no reduction in water clarity. The factors of turbulence (wind induced discolouring) and temperature reductions appear not severe enough to reduce weed quantities; the light limiting effects created by large phytoplankton blooms is also suggested to suppress macrophytes (Brönmark & Weisner 1992). It has now been ascertained that within Drakes reservoir Elodea canadensis is present throughout the year, therefore this must have influences upon the resident organisms and food web structure.
Removal or addition of fish, both resulting in changes of water turbidity, are common ways of manipulating macrophyte growth within a lake. Studies have shown the impact of managing lakes in this way (Lougheed et al. 1998), resulting in significant decreases of vegetation when high stocks of fish are present. It is suggested that the observed condition within the field site (clear water and heavy macrophyte growth) could indicate a potentially low stocking density of fish, especially of the more aggressively feeding common carp.
With and increase of stock density Holopainen et al. (1992) predict a decrease in total zooplankton density; a reduction in the average size of crustacean zooplankton; increased phytoplankton biomass and decreased transparency of water. Results of this magnitude were shown by Vanni (1987); an additional reference to early maturity and reduced sizes of offspring in cladoceran spp. were also suggested.
McQueen (1990) reviews the alternative effects of fish removal - improved water clarity, increased zooplankton populations and heavy macrophyte growth being highlighted. McQueen's predictions are consistent with Drakes reservoir, and although no scientific data has been gathered to substantiate the authors claim of a low stock density, visual evidence is so striking that no other conclusion could be realistic.
Green macrophyte was not present in the stomachs of any fish within this study; the author found this most interesting as he has commonly witnessed the consumption of the same macrophyte by the two species, crucian and common carp, in an aquarium environment. Stomachs did contain small pieces of brown plant material; it is presumed that consumption of these took place through the uptake of detritus. Many authors have cited the presence of aquatic vegetation within the stomachs of carp, but few specify in what state it was observed (reviewed by Crivelli 1983).
With limited availability of microcrustaceans and insect larvae, carp have shown that they can revert to diets of predominantly detrital aggregate, including large quantities of dead macrophytes (Chapman & Fernando 1994). High numbers of zoobenthic and zooplanktonic organisms coupled with an impressive species diversity indicate this to be an unlikely occurrence in Drakes reservoir.
With low quantities of macrophyte the phytoplankton biovolume of a pond increases, but when macrophyte is introduced, and in turn thrives, the phytoplankton biovolume decreases and is replaced by larger bodied cladocerans (Schriver et al. 1995). The results of this study are similar, as few phytoplankton species in very low numbers were present in both stomachs and water samples.
Marked changes within plankton communities have been shown pertaining to ponds with various amounts of macrophyte (Irvine et al. 1989) and/or fish densities (Holopainen et al. 1992). Importantly, Daphnia have been shown to be prominent in clear ponds whereas smaller cladocera thrive in weeded habitats. The plankton trawling exercise revealed small quantities of Daphnia in open water areas, but very few within the stomach contents.
Competition among various sized cladocera has been investigated (Seitz 1980, Demott & Kerfoot 1982, Goulden et al. 1982) and general results show that Daphnia have a tendency to deplete other species of cladocera. A study where Daphnia did fail focused upon the role of their predation via Chaoborus (Sprules 1972). Chaoborus were observed in this study and although absolute quantities are unknown their presence could be an important factor of low Daphnia sightings.
In deeper ponds, the Cyclops is more prone to predation from Chaoborus as they tend to migrate further down the water column than Daphnia (Willoughby 1976); Drakes reservoir is uniformly shallow therefore both species would result in being a prey of Chaoborus. Generally all of these studies have taken place at sites that are not heavily infested with macrophytes.
Importantly, macrophytes have been shown to be an ideal daytime refuge for cladocera when in coexistence with fish, reverting to their most effective grazing in open water at night (Timms & Moss 1984).
4.1.2 Competition and feeding traits of invertebrates in Drakes reservoir
Distinct aspects of competition among cladocerans are common in all waters, but what exactly do these organisms feed on? Populations of large herbivorous Daphnia have the ability to feed on phytoplankton to such magnitudes that they can drastically reduce densities of small cladocerans and rotifers that require the same food source (Vanni 1986). Knisely & Geller (1986) observed that more efficient grazing by all zooplankters occurred in the presence of phytoflagellates (no species were observed in this study); reduced feeding efficiency in the presence of coccales, such as the identified Scenedesmus, is also suggested. The absence of phytoflagellates from this reservoir cannot be scientifically proven within this study; it is proposed that some species do occur, but sampling techniques were ineffective methods of collection.
As mentioned, rotifers may also suffer through the feeding traits of Daphnia. These species may compete for food, but Keratella cochlearis populations are more commonly reduced when swept into the branchial chamber of the Daphnia (Gilbert & Stemberger 1985); on rejection their injuries are commonly to the extent of non-recovery. This is a type of accidental reduction in a population density and it is expected that all rotifers may suffer the same predicament.
The Cypridopsis, a common discovery during the stomach analysis, has thrived among the macrophyte growth within the reservoir; appearances within weed and wall scrapings link them to this environment. Garnett (1965) suggests that these ostracoda are not often accepted as food by many fish species due to their hard outer shell; the results of this experiment clearly show Cypridopsis in 100% of stomachs (sometimes in large quantities). Table 2 indicates that organisms within the group ostracoda contain excellent protein and energy values implying high nutritional rewards for fish that are able to remove the hard bi-valve shell.
One of the very important food resources available to the carp is larval chironomids (Lammens and Hoogenboezem 1991). Mason & Bryant (1975) investigated the feeding traits of these important Chironomid larvae in waters on the Norfolk Broads. They noted that the usually benthic invertebrate frequently migrated up stems of macrophyte to feed upon periphytons (diatoms and filamentous algae); these gave richer sources of amino acids than the silt. This could indicate that a predominately pelagic feeder could also utilise these benthic larvae. Chironomus were identified in both weed and benthic samples thus suggesting similar traits within Drakes reservoir.
Chironomus have also been shown to increase in numbers in line with enlarging communities of submerged macrophytes (Diehl 1988). Mason & Bryant's study showed quantities of filamentous algae inside the stomach of Chironomus; as this algae is a commonly occurring organism within the field site there is a suggestion of a similar food link.
Table 2: The proximate analysis of relevant organisms serving as possible food for crucian carp in Drakes reservoir. This table (adapted from Hepher 1988) brings together the work of over 20 studies to result in approximate nutritional values of the relevant organism groups to this study. Much work has been carried out into protein, lipid and energy levels of specific groups, but carbohydrate appears to be an understudied area.
|*No fieldwork carried out within these areas|
The importance of Chironomus to higher order species varies throughout the year. The energy content of these larvae has been shown to peak in July and then decline to a low in mid-September (Wissing & Hasler 1971). Interestingly, the same study showed that the calorific content of Daphnia was at a low in mid-summer, but increased and peaked in September. It could be suggested that larger fish, which utilise both of these species, would switch in their feeding habits to compensate for these changes.
The reservoir could witness continual shifts in the feeding traits of fish throughout the year. This study revolves around a few weeks only, therefore without further long term investigations the overall feeding patterns can only be a literature backed up opinion.
4.2 Observations into the diet of crucian carp
In summer and early autumn, it has been realised that crucian carp tend to show all the signs of the common cyprinid feeding mode, with a high variation in prey selection (Penttinen & Holopainen 1992). Similar findings appeared within this study as many stomachs contained algae, rotifers, cladocerans, copepods and insect larvae.
As predicted by Hyslop (1980) and Bowen (1983), the identification of the contents within a cyprinid stomach was both difficult and time consuming; the basic digestion process and the grounding by pharyngeal teeth are pinpointed as major causes of this. The main problematic organisms were unsurprisingly the largest, Cyclops and Daphnia, and the softest, Rotifer species; commonly the soft bodied rotifers with their thin cuticles are quickly digested and missed in the gut analysis (Holopainen et al. 1992).
Although the most thorough observations were applied it must be highlighted that errors could have occurred when dealing with these organisms. Samples investigated within one day of capture (hence not frozen) were found to have large numbers of organisms alive. The main species found in this state were Chironomus, Cypridopsis and occasional cladoceran spp.
4.2.1 The role of lower quality food items in the diet of the crucian carp
Previous discussion regarding macrophytes and their possible uptake within detritus resulted in a suggestion that this source of protein is not utilised by the crucian carp within Drakes reservoir due to large numbers of alternative organisms available. Dietary shifts in favour of macrophytes has been shown in certain omnivorous cyprinids (Brabrand 1985); this change is strongly influenced by reductions in alternative food availability as a result of inter and intraspecific competition.
The proximate analysis of the important organism groups is shown in Table 2 and this clearly indicates the significance of an enforced dietary shift from cladocerans to macrophytes; a reduction in protein content of over 40% and energy level of 900 Kcal/kg. These figures indicate that consumption of macrophyte would not be a first or ideal choice for a cyprinid.
It is important to note that detritus was present in all stomachs observed within this study; visual quantities and conditions were similar at the anterior and posterior sections of the gut. Detritus is commonly a mixture of plant debris and amorphous organic matter; this is usually together with the associated heterotrophic and autotrophic microorganisms (Bowen 1976). Bowen's study records that carp do not have a true detritus recycling stomach (lacking in gastric glands) thus suggesting the crucian carp holds very little dependence upon detritus (also indicated in Table 3); this would suggest that the majority is consumed whilst foraging for zoobenthos.
Frequency of occurrence key: *Incidental, **Regular, ***Common, ****Preferred or very high
Ingestion of detritus by crucian carp is not entirely out of the question as this occurrence has been shown under extreme conditions that were attributed to trade-offs generated by the risk of predation (Paszkowski et al. 1996). Table 2 indicates a high-energy value assigned to detritus, but due to the complexity within each individual water body a direct comparison with Drakes reservoir would be inaccurate.
The small quantities of green algae could indicate that these organisms would not be an important source of protein to fish in the size range involved in this study. However, it must be noted that during some period of any fish's life it will rely upon phytoplankton, primarily in early stages of growth (Chakrabarti & Jana 1991).
The majority of cyprinids rely upon secondary producers as food with only the occasional species targeting primary producers (Lammens & Hoogenboezem 1981); phytoplankton with nauplii and rotifers are pinpointed as main food types of 7-8mm first feeding fry (Mark et al. 1897). These suggestions would then indicate that the phytoplankton observed within the stomachs is a by-catch of alternative prey interactions.
The quantities of filamentous algae were more prominent within the stomachs of the crucian carp, but no literature promoting these organisms as an important food source was found. Table 2 suggests that green algae is very low in protein, low in lipids and only provides a mediocre energy level, but as previously discussed, they do provide links to more important organisms within the fishes diet.
One suggestion that does arise is that filamentous algae is taken into the stomach whilst the crucian carp are foraging the macrophytes for migrating chironomid larvae. Filamentous algae are periphytons (attaching themselves to macrophytes) and Mason & Bryant (1975) indicated that chironomid larvae clime from their benthic habitats, up the macrophytes, to feed on these algae. This theory could provide an explanation for why there are large quantities of low nutritional valued filamentous algae within the stomach of the crucian carp.
Although this study does not show a reason for the limited number of diatoms observed the author suggests that they are being out-competed by the macrophytes; diatom growth is typically subject to physical controls (Reynolds 1973) such as turbulence which aids the mixing of nutrients. The vast requirement that macrophytes would have for nutrients would suggest a reason for limited green algae and diatom growth.
The appearance of Arcella in visually large quantities is something of a mystery. No relevant studies containing information on calorific values and frequency of occurrence of this specific species could be found thus suggesting little or no value to the diet of crucian carp. Table 2 gives an indication that energy gained from these protozoans is very high but the vacant spaces show the little work that has been carried out within this field. The author believes that these protozoans are being utilised by the carp in Drakes reservoir as the varied appearance within the gut indicates; a dark black oval shape at the posterior and almost colourless at the anterior.
The importance of rotifers seems inconsequential to fish of the size within this study. Figure 3 showed the dramatic decline in percentage observations as the fork length increases, but as indicated, difficulties in observation could have introduced inaccuracies. It is generally recognised that a cyprinid's diet shift occurs at around 2cm (Mark et al. 1987), 3cm is suggested for crucian carp (Penttinen & Holopainen 1992). Penttinen & Holopainen (1992) study also ascertained that rotifers were an unimportant food item of >5cm crucian carp, but the nutritional values indicated in Table 2 clearly shows why this group is important to juvenile fish.
4.2.2 Important food items and comparisons with previous studies
Generally, all the size ranges of fish were dependent upon cladocera spp. with Chironomus becoming more influential as the fish increased in length (Fig.4 and Fig.5); similar feeding patterns have been shown with Rutilus rutilus (Horpplia 1994), Salmo trutta (Crisp et al. 1978) and Ctenopharyngodon idella (Watkins et al. 1981). Table 2 indicates the excellent nutritional value that both these organisms provide; field studies resulting in carbohydrate figures show the high importance attributed to both groups.
Table 3 shows a high dependence upon micro-crustaceans in comparison to Chironomids. Potentially this could be mis-leading, as although planktonic micro-crustaceans can make up to 50% (carbon weight) of the diet, this is in the gut of 0+ fish, whereas this figure is only 15% in larger fish where Chironomids are more prominent (Penttinen & Holopainen 1992).
Alternatively, the fishes' dependence upon chironomid larvae does not only increase with fork length, the size of the larvae is also influential. The common carp is predominately a benthic feeder, and as Fig. 23 indicates, it has an increased foraging ability as it grows in length, allowing the fish to extract larger more deeply imbedded larvae. This feeding application will allow the common carp to utilise larger and more nutritional organisms unavailable to the crucian carp thus giving it a competitive advantage.
Penttinen & Holopainen (1992) investigated feeding activity within crucian
carp communities and although there are noticeable similarities with this
study, certain marked differences within length ranges are apparent. For
example, their fish stock were consuming benthic cladocerans and Chironomus
when they were as small as <3cm in length, whereas this study showed that
on average, fish >12.2cm were more dependant on these organisms with little
or no sign of them being in stomachs belonging to fish <11.7cm. They also
showed a notable absence of benthic cladocerans in the diet of fish >10cm;
this study shows an increased uptake as fish become larger.
Paszkowski et al. (1996) showed higher quantities of Chironomus in larger crucian carp and benthic cladocerans in smaller, but little or no pelagic cladocerans. Again this shows a slight variation in food choice, but with so many similarities, it is implied that these separate communities of crucian carp are making best use of their habitat.
Most fish species do vary feeding rates, territories and adapt broader diets in response to low or fluctuating food availability within their individual habitats (Dill 1983, Lammens & Hoogenboezem 1981). The importance of specific prey taxa varies greatly between lakes, and individual crucian carp from a single lake may contain a wide range of types and sizes of foods (Paszkowski et al. 1989).
The limited observations of Cyclops within the water samples may be attributed to the intense growth of macrophytes (Hansen & Jeppesen 1992); as mentioned this would lead to a reduction in phytoplankton, a valuable food source to the Cyclops. Interestingly, the same author notes that the jerky motion of the Cyclops is an effective predator avoidance technique; small numbers within the investigated stomachs could be a result of this defence.
The difficulty in catching Cyclops, in comparison with cladocerans is highlighted by Winfield et al. (1983) in an experiment using two cyprinid species. The study showed a large difference in the capture success when involving these two invertebrates. The evidence of these two studies indicate that the Cyclops is not a chosen food item by many fish species; prey items requiring less energetic capture methods would first be selected.
This study suggests that cladocera spp. and chironomid larvae are most likely to be the preferred diets of the crucian carp (>11.2cm) in Drakes reservoir. There could be a number of reasons for this choice which include competition of both inter and intraspecific nature, visual capabilities of the fish, escape capabilities of the prey, food abundance and preferred feeding methods.
4.2.3 Competition among the fish community in Drakes reservoir
The subject of competition has been suggested throughout this study and the author has no doubt that there would be competition amongst the fish within Drakes reservoir. Crucian carp, when in small ponds, have a tendency to stunt (Fig.24) causing large quantities of 8-15cm fish (Holopainen & Pitkanen 1985); the author has witnessed this occurrence in over ten ponds in England.
Other closely related cyprinids have also been seen to reduce growth when in a high stock densities, competing for lower quantities of natural food (Hulata et al. 1982). A heavily compacted population of small crucian carp has been shown to be very aggressive in their feeding and interference of others within the same community (Paszkowski et al. 1990); also larger crucian carp show an exploitative advantage. This evidence suggests the likelihood of intraspecific competition whereas interspecific competition (involving the common carp) cannot be easily proved, but with the similar feeding preferences indicated within Table 3, it could be presumed this also occurs.
No visually deepened fish were observed within this study; this was due to the non-existence of piscivores hence the fitness cost associated with defence was not an issue. Deeper more cumbersome fish are commonly out-competed for food (Pettersson & Brönmark 1997); these fish would require a larger intake of nutritional food to sustain their larger body mass.
One of the more obvious reasons for certain choices in prey would be that of actual prey size (this was discussed previously in relation to chironomids). Paszkowski et al. (1989) studied this relationship between body and food size of the crucian carp. Figure 26 shows the relevant results from their study, those that directly relate to the fish size within Drakes reservoir. From these graphs it becomes apparent that there is an ontogenetic shift in prey size with the larger fish becoming more selective and in turn taking larger prey. On the whole this is not surprising and certain links can be made with Drakes reservoir; increase fork lengths revealed increased prey size (Fig.4, Fig.6 and A.affinis in Fig.5). Fish of 13cm in the Paszkowski et al. (1989) study showed preferences for prey longer than 4mm (4000µm) whereas the crucian carp community in Drakes reservoir yielded no prey over 1.4mm (1400µm).
Drakes reservoir is a twin species community and Fig. 23 showed how the common carp preferred a diet of chironomids >4mm; these two studies in conjunction with the results from Drakes reservoir could suggest interspecific competition, with the crucian carp losing out to the larger common carp.
Interestingly, crucian carp (11-14cm) have the ability to ingest zooplankton >200µm, with Penttinen & Holopainen (1992) finding planktonic cladocera of 4-600µm most frequently within the guts of their fish. No cladocera approaching 50% of this size were observed within Drakes reservoir indicating that the previous suggestion of high macrophyte growth suppressing the size of cladocera may well be an occurrence (Irvine et al. 1989).
Pettersson & Brönmark (1993) studied the changes crucian carp made in their foraging habits when hungry vs. fed and with predator vs. without. Even when hungry, the crucian carp rarely traded off safety against feeding in the presence of predators. This is not surprising, but when predators were not present, increased excursions from weed beds into open water were more common. These behaviours could help understand why few open water invertebrates were prevalent within the stomachs.
The diversity of organisms within the reservoir, many of which reside in and around the macrophyte, leads the author to believe that only rarely do these small fish risk movement from the safety of the weed beds. The huge quantities of macrophyte would supply enough cover for the crucian carp to forage safely without having to take risks in catching larger, less abundant prey.
4.2.4 Niche overlaps within the fish community
The final point of discussion involves the possibility of niche overlaps between both resident fish species. The food types found within the stomachs of the crucian carp would certainly indicate an omnivorous nature, pelagic feeding throughout their life, but a dependence upon benthic interactions becoming more important as the fish increases in size.
The large quantities of cladocera spp. within all stomachs could indicate a shift in diet to compensate for the feeding habits of the common carp, which is predominately benthivoruos. No distinct switches in the diet of crucian carp are known, but a gradual ontogenetic shift in the dominance of food items has been shown within different size classes (Penttinen & Holopainen 1992). They have also been shown to be less effective at judging rewards associated with single prey items (Paszkowski et al.1989).
Although no specific literature directly compares these, the data from
Drakes reservoir plus all the aforementioned literature lead the author
to believe that a niche overlap is present within the reservoir. This
overlap, which is predominately benthic, has forced a shift in prey choice
leaving the crucian carp to feed on smaller pelagic organisms. The crucian
carp have managed to adapt due to their generalistic feeding nature thus
allowing a switch to alternative prey; this is helped by the healthy species
diversity within the reservoir.
This study has explored the aquatic interactions between the invertebrates and fish species within Drakes reservoir and has resulted in a knowledge of the crucian carps' feeding habits and preferences.
A large quantity of macrophyte is present throughout the year, this is due to limited turbulence and the low fluctuations in temperature, it is also suggested there is a low stocking density of fish. Results suggest that crucian carp have a high variation in prey selection, no green macrophyte was present in the stomachs, however dead leaf material was observed. Crucian carp do eat macrophyte when the overall species diversity is low in a lake, this is not the case in Drakes reservoir.
Low quantities of phytoplankton were observed which is common in pools with heavy macrophyte growth, commonly cladocerans will fill this available niche by using the macrophyte as a refuge, it is suggested to be the case in Drakes reservoir. Green algae is thought not to be an important source of protein to the crucian carp, those observed are suggested to be an inevitable by-catch of normal feeding behaviour. Large quantities of filamentous algae was present in all stomachs, it is believed that this is a by-catch of the fish grazing on chironomid larvae within the macrophyte.
Detritus was present in all stomachs, it is suggested this is taken up whilst foraging for zoobenthos and is not utilised by the fish. Contrary to published opinion, Cypridopsis are being eaten by the crucians, thus showing no difficulty in removing their bi-valve shell. Arcella are also being utilised but the dependence upon these protozoans is not clear; rotifers are not important to the fish of the size in this study.
The crucian carp in Drakes reservoir are omnivorous, they are pelagic feeders throughout their life, but turn to benthic species as the fish increases in length. The threat of less weeded areas could explain the lack of larger invertebrates in the diet, but the preferred food items of the crucian carp (>11.2cm) did include small cladocera species, both benthic and pelagic plus chironomid larvae. Common carp also have a preference for chironomid larvae, thus suggesting of interspecific competition. The large quantities of cladocera in the stomachs indicate a shift in diet by the crucian carp to compensate for this. This does indicate that a niche overlap is present, but the generalistic feeding nature of the crucian carp has allowed a switch to these alternative food sources. The stunted nature of the crucian carp also indicates the occurrence of intraspecific competition in the reservoir.
I wish to thank Dr Russell, Mr R. Moate, Mr Griffiths, and Mr G. Carter, University of Plymouth for their help in producing the photographic images required for the completion of this study. Also my colleagues Jonathon Morley and Jonathon Clarke for their opinions on this manuscript and Pete Walton for his proof reading. I would also like to thank Dr Simon Davy and Dr Malcolm Findlay, Institute of marine studies, University of Plymouth for their guidance and opinions and finally Mr Ian McCulloch, freshwater biological association library.
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