Trophic Position of Two Mysid Species (Crustacea: Mysidacea) in an Estuarine Ecosystem in Auckland, New Zealand, Using Stable Isotopic Analysis
1Department of Zoology, The Open University of Sri Lanka, Nawala, Nugegoda, Sri Lanka
The trophic position of an organism can be determined by the stable isotope studies of nitrogen and carbon. The main objective of this study was to determine the trophic position of two mysid species, Tenagomysis chiltoni and T. novaezealandiae in the Kakamatua stream ecosystem in using 13C and 15N isotopes. Samples were collected during two weeks period in late December 2008 and early January 2009 including primary producers, leaf litter, aquatic invertebrates, fish species and sediment samples. Aquatic invertebrates and fish were collected from the stream using a hand net. Litter samples were collected randomly from the stream floor. Samples were sealed in plastic bags, and stored in a freezer until processing. All the samples were oven-dried, then ground to obtain a homogeneous powder. Three replicates of each sample were prepared. Samples were processed by the Waikato Stable Isotope Unit, of , . A trophic-level effect of 13C and 15N enrichment was clearly observed. Stable isotopic data indicated that T. chiltoni and T. novaezealandiae exhibited variety of feeding habits (feeding on the first and the second trophic levels) and can be considered as omnivores. Among the other invertebrates analysed, mysids seem to be an important invertebrate fauna which are capable of energy transferring towards the higher trophic level both from primary food sources and the secondary consumers as well. Differences in the isotopic composition were observed among same species depending upon the ontogenetic development.
At a glance: Figures
Keywords: nitrogen isotope, carbon isotope format, food web analysis, estuary, New Zealand
American Journal of Marine Science, 2013 1 (1),
Received September 13, 2013; Revised October 22, 2013; Accepted October 23, 2013Copyright © 2014 Science and Education Publishing. All Rights Reserved.
Cite this article:
- Punchihewa, N.N., and S.R. Krishnarajah. "Trophic Position of Two Mysid Species (Crustacea: Mysidacea) in an Estuarine Ecosystem in Auckland, New Zealand, Using Stable Isotopic Analysis." American Journal of Marine Science 1.1 (2013): 22-27.
- Punchihewa, N. , & Krishnarajah, S. (2013). Trophic Position of Two Mysid Species (Crustacea: Mysidacea) in an Estuarine Ecosystem in Auckland, New Zealand, Using Stable Isotopic Analysis. American Journal of Marine Science, 1(1), 22-27.
- Punchihewa, N.N., and S.R. Krishnarajah. "Trophic Position of Two Mysid Species (Crustacea: Mysidacea) in an Estuarine Ecosystem in Auckland, New Zealand, Using Stable Isotopic Analysis." American Journal of Marine Science 1, no. 1 (2013): 22-27.
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Mysids are small crustaceans which show high abundance in estuarine waters. Consequently, they serve as a major food source for ecologically and commercially important fish species which use estuary as nursery grounds. Thereby, they become an important link in estuarine food chains.
Stable isotope analysis (SIA) can provide a measure of trophic position, which integrates the assimilation of energy flow (or mass) through all the possible trophic pathways leading to an organism . This analysis may not necessarily reflects short term feeding patterns and it provides an effective tool for integrating long-term assimilation of nutrients . Therefore more traditional methods of gut content analysis have several draw backs, notably some organisms digest their prey quickly, making identification difficult, and this method reflects immediate feeding (if the diet is in an undigested state) pattern only . In such cases, SIA can provide a useful alternative tool and give an insight into the feeding relationships between the organisms within a given food web [4, 5].
SIA approach has been successfully applied to the study trophic interactions in variety of organisms, including mysids and zooplankton [2, 6, 7, 8, 9]. SIA is achieved by using isotopic fractionation of carbon, nitrogen and sulphur. The stable isotopes are different sizes and one is heavier than the other (e.g.: 12C and 13C, 13C is 8.3% heavier than 12C). Many reactions alter the ratio of heavy to light isotope, or “fractionate” stable isotopes, and however, the degree of fractionation is typically quite small . In biological processes, when inorganic carbon is used to make organic compounds, 12C is weakly bonded and reacts more readily than 13C, because of its lighter mass. The level of this isotope effect is expressed as a fractionation factor. Therefore, the isotopic fractionation is the fluctuation in the isotope ratios as a result of natural biochemical processes due to their differences in atomic mass. Most ecological studies express isotopic composition in terms of δ values, which are parts per thousand (‰) differences from a reference standard .
The carbon isotopic compositions of the whole body of an animal reflects the isotopic composition of its diet, but the animal is on average enriched in δ13C by about 1 ‰ relative to the diet values. However, the δ13C values of whole bodies of individuals of a species raised on the same diet may differ by up to 2 ‰ .
The relationship between the 13C /12C ratio of a tissue and the 13C /12C ratio of the diet depends both on the type of tissue and the nature of the diet . Many of the isotopic relationships among the major biochemical fractions, namely the lipid, carbohydrate and protein fractions are qualitatively preserved as diet carbon is incorporated into the animal. However, the difference between the δ13C values of a biochemical fraction in an animal and in its diet may be as large as 3 ‰ .
The δ 15N and δ13C contents of animals reflect their diets. The ratio of stable isotopes of nitrogen (δ 15N) can be used to estimate trophic position because the δ 15N of a consumer is typically enriched by 3–4 ‰ relative to its diet [4, 10]. Enrichment of δ 15N through the trophic network is widely recognized among most animals, including invertebrates and vertebrates, leading to a value of 3·4 ± 1·1‰ [4, 11].
Stable isotope studies on mysid feeding relationships are rare. However, several world-wide studies using stable isotopic analysis of different mysid species have been reported [2, 8, 12, 13, 14]. The isotopic data of Paramysis lacustris Czerniavsky, from Curonian lagoon, suggested that diet changes occurs during ontogenetic development . The isotopic signatures of the prey of M. relicta in  showed 25% feeding on amphipod parts and 20% on phytoplankton. The remainder of the diet consisted of zooplankton and rotifers. Stable isotope δ 13C, δ 15N values of the winter diets of M. mixta and M. relicta determined that they exploit both benthic and pelagic habitats . These facts suggest that isotopic composition of aquatic organisms can provide basic information on their food source and trophic level. In theory, we can thus construct a SI food web (δ 15N versus δ 13C) of an ecosystem.
The main objective of this study is to determine the trophic position of two mysid species, Tenagomysis chiltoni and T. novaezealandiae in an estuarine ecosystem. To realize this goal, isotopic ecological structure was determined in a estuarine ecosystem in Greater Auckland region using 13C and 15N isotopes.
Kakamatua Stream is situated in the west coast of Auckland region (Figure 1) and one of the major waterways on the northern side of the Manukau Harbour, into which it drains. It has most mature and dense riparian vegetation and reed beds along the stream. Samplings were performed at the lower reaches of this stream, which inundated by the tidal action.
The mysid species T. chiltoni and T. novaezealandiae dominated in this site, sympatrically with the glass shrimp (Palaemon affinis). The most common fish population at this site was Inanga- whitebait (Galaxias maculates). In addition juvenile short finned eel ( australis), Flat fish (flounder) and Athrinidae sp. (hardy heads) were rarely caught at this site.
Samples were collected in late December 2008 and early January 2009 including primary producers (Ulva sp., filamentous green algae and grass), leaf litter (terrestrial), consumers (aquatic invertebrates: amphipods, isopods, mollusc, decapods, mysids), fish and sediment samples. Samples were sealed in plastic bags, and stored in a freezer (−20°C) until processing. Aquatic invertebrates and fish were collected from the stream by a hand net. Litter samples were collected randomly from the stream floor. Surface sediments were collected by using a core sampler.
All the samples were oven-dried to a constant weight at 40°C, then ground in an Agatha stone mortar and pestle to obtain a homogeneous powder. For the fishes, only the muscle parts was used for the analysis.Three replicates of each sample were prepared and the whole body of the animal samples was considered. The plant and animal samples of approximately 20 mg and sediment samples of 200 mg were processed by the Waikato Stable Isotope Unit, University of Waikato, Hamilton, New Zealand.
The carbon value (δ13C) was measured to a precision of ±0.1% and samples were referenced to a precalibrated C4 sucrose standard that was cross-referenced to the Pee Dee belemnite standard . The nitrogen value δ15N was measured to a precision of ± 3%, and samples were referenced to an urea standard which was traceable to atmospheric nitrogen .
The ratios of 13C/12C and 15N/14N (13C, 15N- heavy isotope; 12C, 14N- light isotope) are expressed as relative difference using the following equations.
Where δ13C and δ15N is the isotopic compositions referenced to the standards. 13C/ 12Csample and15N/14N sample is the isotopic composition of the sample. 13C/ 12C standard and 15N/14Nstandard is the isotopic composition of the standard.
The stable isotope values of δ15N and δ13C were used to visualise the trophic position of each link (carbon and nitrogen sources) of the Kakamatua Stream ecosystem.
The δ13C and δ15N mean (± SD) stable isotopic values of animals and their diets are given in Figure 2. These values demonstrate a separation between producers and consumers, and the evidence of δ13C and δ15N enrichment with increasing trophic level. It is important that these values demonstrate a noticeable separation between allochthonous (A & C-terrestrial) and autochthonous (B-in-stream) samples collected from this ecosystem (Figure 2).Leaf litter (allochthonous) had the most depleted δ13C values and lower δ15N values among the samples which were collected from the ecosystem (Table 1). The mineral soils are more enriched with δ13C and δ15N than the leaf litter (Table 1).
The grass which were collected from the boundary of the stream, showed more enriched 13C values than the aquatic primary producers (Ulva sp., filamentous algae) in-stream. The opposite is true for δ 15N values. Ulva sp. and filamentous algae more enriched with 15N than the terrestrial primary producer, grass (Table 1).
The δ13C values of invertebrates ranged from –24.22 to –20.06‰. Among the animals collected from the stream, the moluscs gave rather high δ13C values (δ13C −13.57 to −12.29 ‰) than all the other samples. The δ13C values of fish ranged from, –22.49 to–17.73 ‰ (Table 1).
The δ15N value of invertebrates varied from 8·35 to 12.5‰. It is increased in the following order: Isopod, palamonid shrimp, amphipods, mud crab, T. novaezealandiae, adult T. chiltoni and juvenile T. chiltoni. The increasing order of δ15N values of fish species: Athrinidae sp., Juvenile G. maculates, adult G. maculates, juvenial flounder and juvenile A. australis (Table 1).
Among these primary consumers T. novaezealandiae were more enriched with 13C and T. chiltoni were more enriched with 15N values. It is significant that T. chiltoni adults are more enriched with δ15N values and δ13C values than their juveniles. When analysing the isotope values related with the above hypothesis, the most possible common food links of both mysid species appear as isopods, filamentous algae and amphipods (Table 1).
The higher tropic level (secondary consumers) represented higher δ15N values than other tropic levels, it mainly consist of fish. The juvenile short finned eel (A. australis) is the most 15N enriched link (δ15N 15.04 to 14.87 ‰) and the juvenile flounder is the highest 13C enriched (δ13C−18.00 to −17.73 ‰) link among the fish. Similar to other fish G. maculates also indicated higher δ15N values (δ15N 12.9 to 13.6 ‰). Juvenile G. maculates show lower δ15N values than their adults. However, the juvenile Athrinid sp. has significantly lower δ15N values (δ15N 10.92 to 11.09 ‰) than other fish species, which is similar to the values of primary consumers (Table 1).
The stable isotopic signatures of different food links facilitated the identification of trophic pathways and the trophic position of mysid species in Kakamatua Stream. Overall δ13C measurements ranged from between −31.6 ‰ (±0.62) for leaf litter and −12.95 ‰ (±0.64) for molluscs, and δ15N values ranged from between −0.9 ‰ (±1.02) for leaf litter and 14.96 ‰ (±0.09) for juvenile short finned eel (A. australis).4.1. First Trophic Level
Depending on the hypothesis of differences in δ15N value between the consumer and the diet, a consumer is typically enriched by 3–4 ‰ relative to its diet [1, 4, 11] and thus the primary food link and the primary consumers should have a difference of δ15N values between 3-4 ‰. On the argument of the differences in δ13C value between the consumer and the diet, the consumer is enriched up to by 1 ‰ and it may be large as 3 ‰ relative to the food sources .
Therefore, based on isotopic signatures, the first trophic levels mainly supporting the primary consumers are identified as algae and sediments. The δ15N values of leaf litter collected from the stream do not fit into the above hypothesis as potential food source of collected primary consumers. The filamentous green algae and Ulva sp. had more enriched 15N values than sediments. The filamentous algae had higher enrichment of δ13C than other aquatic primary food sources, is in agreement with δ13C values that have been reported for filamentous green algae of different stream ecosystems in .
The invertebrates in Kakamatua except mollusc were more dependent on autochthonous (in-stream) carbon sources (Ulva sp., filamentous green algae), and this is similar to the previous results of , in which insects from adjacent grassland streams mainly depend on autochthonous material. Therefore the aquatic inputs mainly Ulva sp. and, filamentous green algae sustain the aquatic food web at Kakamatua stream.
The results suggest a dependency of invertebrates on aquatic food sources rather than terrestrial leaf litter. Regardless, the stream ecosystem is not directly supported by the detritus based food chain. Because, the collected leaf litter samples offered depleted 13C and 15N values and could not be able to support the invertebrate groups which were collected for the analysis, though different invertebrate groups or different types of leaf litter may lead to the detritus based food chain. However, most of the primary consumers; amphipods, isopods, H. crassa, P. curvirostris, and T. chiltoni feed on sediments, the high nutrient, muddy substrates, which suggests sediments (substrate) may trap nutrients from detritus and make them available to the stream fauna. This is evident from the isotopic values of sediments, and it indicates higher 13C and 15N enrichment than the leaf litter. This argument agrees with a study of the trophic interactions within an estuarine food web (northern ) using fatty acid biomarkers and stable isotopes . Finally it can be suggested that both autochthonous and allochthonous leaf litter-derived nutrients in sediments may be available to invertebrates. This agrees with a New Zealand stable isotopic study , which indicated that the food webs of pasture streams are based on both autochthonous and allochthonous material.4.2. Second Trophic Level
Based on the isotopic signatures of invertebrates molluscs can be categorized as a different trophic group due to their extremely high 13C values than other invertebrates. Further to that, among the food sources analysed, grass is the possible food source for mollusc which shows higher δ13C values. Therefore, based on the hypothesis of differences in δ15N value and δ13C values (DeNiro & Epstein; 1981; 1978), molluscs and grass (diet) can be considered as an entirely separate trophic relationship.
Depending on the differences of both δ13C and δ15N values, each consumer and their most potential food source/s can be assigned as: P. curvirostris (shrimp) - sediments; Amphipods - Ulva sp. and sediments; juvenile T. chiltoni - Ulva sp. and sediments; Austridotea anectens (isopod) - sediments; juvenile Helice crassa (mud crab) - sediments; adult T. chiltoni - filamentous algae, Ulva sp. sediments, amphipods and isopods; T. novaezealandiae - filamentous algae, isopods, and amphipods; molluscs – grass.
Stable isotopic data indicated that T. chiltoni and T. novaezealandiae exhibited variety of feeding habits and can be considered as omnivores. This stable isotopic data is supported by the gut content analysis of T. chiltoni in Lake Ellesmere , where the ingested foods had both aquatic and terrestrial origin (both from primary and secondary trophic levels).
Depending on the differences of δ13C and δ15N values for juvenile T. chiltoni and adult T. chiltoni, it is apparent that their food preference were also different, juvenile T. chiltoni fully depended on herbivorous diet (Ulva sp.) and adults are omnivores (filamentous algae, Ulva sp, sediments, amphipods and isopods). Similar observations on mysid diet changes during ontogenetic development have been demonstrated by several studies [19, 20, 21] and the findings here agrees with a stable isotope study of Paramysis lacustris . Thus, the significant enrichment of δ 15N values and δ13C values of T. chiltoni with the increasing size is in aggrement with the similar observations of P. lacustris . Similarly, enrichment of δ 15N values of T. chiltoni than T. novaezealandiae reflects that larger the size of mysids (even the different species), the enrichment of δ 15N value also higher and larger mysid species probably depends on more varities of food than smaller.
Among the other invertebrates analysed, mysids are an important intermediate link of this ecosystem and capable of energy transfer towards the higher trophic level both from primary food sources and the secondary consumers as well. Therefore, this study provides the evidence that mysids depend on variety of food items, and also if abundant they can have a substantial effect on energy transfer at all trophic levels.4.3. Third Trophic Level
Differences in the isotopic composition were observed among same species (G. maculates) depending upon the ontogenatic development, juvenile galaxid showed comparatively low isotopic compositions (δ15N δ13C values) than adult galaxid. Based on the differences of δ13C and δ15N values, the potential food sources of juvenile A. australis are T. chiltoni, T. novaezealandiae and juvenile G. maculates. Similarly, the likly food sources which closely link with G. maculates are T. chiltoni, T. novaezealandiae, isopods and amphipods while juvenile G. maculates link with juvenile T. chiltoni and amphipods. The δ13C and δ15N values of flat fish closely link with the isotope values of T. novaezealandiae and isopods as their potential food sources, as explained earlier, depending upon their lower δ15N values. Athrinidae sp. do not link with any food item collected from the ecosystem.
The juvenile short finned eel has the highest enriched δ15N values and is the top carnivore. Similar results have been reported from short finned eels in the . The juvenile fishes captured from the stream displayed a variety of δ13C and δ15N values, presumably reflecting a wide variety of food sources at different trophic positions . The present study shows that the juvenile short finned eel displayed different trophic positions, as a top carnivore in the fourth trophic level (feeding on the second trophic level) and in the third trophic level (feeding on T. chiltoni, T. novaezealandiae and juvenile G. maculates at second or third trophic levels). Similar observations on the short finned eels which fed on T. chiltoni and G. maculates in a lake in New Zealand  and juveniles of short finned eel contained mysids in their diet as the second most common food .
Galaxius maculates also exhibits different trophic positions in the third and fourth trophic level. The juvenile flounder is the highest carbon enriched link among the fish and closely link with mysids. It is in agreement with similar stable isotopic between flounder and mysids .
The stable isotopic signature of juveniles and adult G. maculates showed that they fed at different trophic levels; juveniles feed on juvenile T. chiltoni while adults feed on adult T. chiltoni. This agrees with the observation of , that the juvenile spotted flounder contained a greater number of mysids in their stomachs while in larger fish, decapods and some fishes were more abundant in their stomachs.
The δ13C and δ15N values demonstrate a separation between producers and consumers, and the evidence of δ13C and δ15N enrichment with increasing trophic level. It is important that these values demonstrate a noticeable separation between allochthonous (terrestrial) and autochthonous (in-stream) samples collected from this ecosystem.
Leaf litter had the most depleted δ13C values and lower δ15N values among the samples which were collected from the ecosystem. Grass which were collected from the boundary of the stream, show more enriched 13C values than the aquatic primary producers (Ulva sp., filamentous algae) in-stream. The opposite is true for15N value: Ulva sp. and filamentous algae more enriched with 15N than the terrestrial primary producer, grass. Among the samples collected from the stream, the moluscs gave the highest δ13C values.
T. chiltoni and T. novaezealandiae exhibited variety of feeding habits, feeding on the first and the second trophic levels and can be considered as omnivores. Among the other invertebrates analysed, mysids seem to be an important invertebrate fauna which are capable of energy transferring towards the higher trophic level both from primary food sources and the secondary consumers as well. Differences in the isotopic composition were observed among same species depending upon the ontogenatic development.
Using the stable isotopic values of collected food links and their trophic positions, the achievable food web for Kakamatua Stream is illustrated in Figure 3.
This project was funded by the Auckland University of Technology, Auckland, New Zealand.
|||Peterson, B. J., Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review of Ecological Systems, 18, 293-320.|
|||Johansson, O. E., Leggett, M. F., Rudstam, L. G., Servos, M. R., Mohammadian, M. L., Gal, G., et al. (2001). Diet of Mysis relicta in Lake Ontario as revealed by stable isotope and gut content analysis. Canadian Journal of Fishery and Aquatic Sciences, 58, 1975-1986.|
|||Mauchline, J. (1980). The biology of mysids and euphausids. In J. H. S. Blaxter, Russell, F. S., Yonge, M (Ed.), Advances in marine biology (Vol. 18, pp. 3-369).|
|||Minagawa, M., Wada, E. (1984). Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta, 48, 1135-1140.|
|||Post, D. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83, 703-718.|
|||Toda, H., Wada, E. (1990). Use of 15N/14N rations to evaluate the food source of the mysid, Neomysis intermedia Czerniawsky, in a eutrophic lake in Japan. Hydrobiologia, 194, 85-90.|
|||Hansson, S. H., J. E Elmgren, R. Larsson, U. Fry B. Johansson, S. (1997). The stable nitrogen isotope ratio as a marker of food-web interactions and fish migration. Ecology 78, 2249-2257.|
|||Gorokhova, E., & Hansson, S. (1999). An experimental study on variations in stable carbon and nitrogen isotope fractionation during growth of Mysis mite and Neomysis integer. Canadian Journal of Fishery and Aquatic Sciences, 56, 2203-2210.|
|||Branstrator, D. K., Cabana, G., Mazumder A., Rasmussen, J.B. (2000). Measuring Life-history omnivory in the opossum shrimp, Mysid relicta, with stable nitrogen isotopes Limnology and Oceanography, 45, 463-467.|
|||DeNiro, M. J., & Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42, 495-506.|
|||DeNiro, M. J., & Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta, 42, 495-506.|
|||Mulkins, L. M., Jelinski, D. E., Karagatzides. J. D., & Car, R A. (2002). Carbon isotope composition of mysids at a terrestrial-marine ecotone, Clayoquot Sound, British Columbia, Canada. Estuarine, Coastal and Shelf Science, 54 (4), 669-675.|
|||Lesutienė, J., Gorokhova, E., Gasiunaite, Z. R., & Razinkovas, A. (2007). Isotopic evidence for zooplankton as an important food source for the mysid Paramysis lacustris in the Curonian Lagoon, the south-east ern Baltic Sea. Estuarine, Coastal and Shelf Science, 73 (1-2), 73-80.|
|||Lehtiniemi, M., Kiljunen, M., & Jones, R. I. (2009). Winter food utilisation by sympatric mysids in the Baltic Sea, studied by combined gut content and stable isotope analyses. Marine Biology, 156, 619-628.|
|||Hicks, B. J. (1997). Food webs in forest and pasture streams in the Waikato region: a study based on analyses of stable isotopes of carbon and nitrogen, and fish gut contents. New Zealand Journal of Marine and Freshwater Research, 31, 651-664.|
|||Rounick, J. S., Winterbourn, M. J., Lyon, G. L. (1982). Differential utilisation of allochthonous and autochthonous inputs by aquatic invertebrates in some New Zealand streams: a stable carbon isotope study Oikos, 39, 191-198.|
|||Alfaro, A. C., Thomas, F., Sergent, L., Duxbury, M. (2006). Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuarine, Coastal and Shelf Science, 70, 271-286.|
|||Waite, R. P. (1980). Food resource utilization by Tenagomysis chiltoni (Crustacea: Mysidacea). MSc. Thesis, University of Canterbury. 155pp.|
|||Branstrator, D. K., Cabana, G., Mazumder A., & Rasmussen, J. B. (2000). Measuring life history omnivory in the opossum shrimp, Mysis relicta, with stable nitrogen isotopes. Limnology and Oceanography, 45, 463-467.|
|||Viherluoto, M., Kuosa, H., Flinkman, J., & Viitasalo, M. (2000). Food utilisation of pelagic mysids, Mysis mixta and M. relicta, during their growing season in the northern Baltic Sea. Marine Biology, 136, 553-559.|
|||Viherluoto, M., & Viitasalo, M. (2001). Temporal variability in functional responses and prey selectivity of the pelagic mysid, Mysis mixta, in natural prey assemblages. Marine Biology, 138, 575-583.|
|||Kelly, D. J., Jellyman, D. J. (2007). Changes in trophic linkages to shortfin eels (Anguilla australis) since the collapse of submerged macrophytes in Lake Ellesmere, New Zealand Hydrobiologia, 579, 161-173.|
|||James, G. D., & Unwin, M. J. (1996). Diet of Chinook salmon (Oncorhynchus tshawytscha) in Canterbury coastal waters, New Zealand. New Zealand Journal of Marine and Freshwater Research, 30, 69-78.|
|||Ryan, P. A. (1986). Seasonal and size-related changes in the food of the short-finned eel, Anguilla australis in Lake Ellesmere, Canterbury, New Zealand. Enviromental biology of fishes, 15(1), 47-58.|
|||Webb, B. F. (1973). Fish populations of the Avon-Heathcote Estuary. 3. Gut contents. New Zealand Journal of Marine and Freshwater Research, 7, 223-234.|
|||Redon, M. J., Morte, M. S., Sanz-Brau, A. (1994). Feeding habits of the spotted flounder Citharus linguatula off the eastern coast of Spain. Marine Biology, 120, 197-201.|
|||Craig, H. (1957). Isotopic standards for carbon and oxygen and correction factors for mass spectrometric analysis of carbon dioxide Geochemica Cosmochimica Acta, 12, 181-186.|
|||Mariotti, A. (1983). Atmospheric nitrogen is a reliable standard for natural 15N abundance measurements. Nature, 303, 685-687.|