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Article in Ecology of Freshwater Fish · December 2006 DOI: 10.1111/j.1600-0633.2006.00191.x · Source: OAI

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Murray cod an apex predator in the Murray River, Australia

Brendan Ebner. Murray cod an apex predator in the Murray River, B. Ebner1,2 Australia 1Cooperative Research Centre for Freshwater Ecology of Freshwater Fish 2006: 15: 510–520. 2006 The Author. Ecology, Murray-Darling Freshwater Research Journal compilation 2006 Blackwell Munksgaard Centre, Lower Basin Laboratory, Mildura, Aus- tralia, 2Department of Environmental Manage- ment and Ecology, La Trobe University, Abstract – To determine if the Murray cod Maccullochella peelii peelii is Wodonga, , Australia an apex predator in the lowland rivers of the Murray-Darling Basin, its feeding ecology was compared with that of the sympatric top predator, golden perch ambigua ambigua based on samples supplied by recreational anglers. Diet and prey size were reconstructed from alimentary tract contents of Murray cod (N ¼ 39) and golden perch (N ¼ 52), and their feeding morphology was assessed and included calculation of length– gape relationships and relative gut index. Both fed principally on Key words: apex predator; top predator; Murray- fish and decapods although Murray cod was the more piscivorous Darling Basin; Maccullochella; Macquaria (frequency of occurrence 44% versus 6%, total number 50% versus 2%, Brendan Ebner, Wildlife Research and Monitor- total weight 90.4% versus 16.0%). Based on reconstructions of prey sizes, ing, Environment ACT, PO Box 144, Lyneham, fishes up to 1 kg in weight were preyed on by Murray cod, distinguishing it ACT, 2602, Australia; from other top predatory fishes in the Murray-Darling Basin and e-mail [email protected] supporting its classification as an apex predator. Accepted for publication June 22, 2006

Australia, Crabb 1997) does not support any partic- Introduction ularly large predatory mammals or reptiles (e.g. bears Species are classified into trophic guilds based on in the Northern Hemisphere, crocodilians in the information including feeding behaviour, ecomorphol- tropics) that feed on fish (e.g. Walker 1986). Accord- ogy, foraging habitat and diet, in order to simplify food ing to current classification (Harris 1995a; Schiller & webs and develop an understanding of trophic processes Harris 2001; also see Gehrke & Harris 2004), five and ecosystem structure (Lindeman 1942; Stephens & native species of fish are top predators in the fish Krebs 1986). Whilst this approach has limitations, it has community of the Murray-Darling Basin. Quantitative proven useful in the identification of important information supports this classification in relation to ecological processes including trophic cascades freshwater catfish Tandanus tandanus (Davis 1977) (Gerking 1994) and competition for resources (Mittel- and golden perch Macquaria ambigua ambigua bach & Chesson 1987; Persson 1994; Yodzis 2001). (Battaglene 1991), though not Hyrtl’s tandan Neosilu- Species that consume prey from more than one trophic rus hyrtlii (Pusey et al. 1995, 2000). The latter is more level make grouping species into trophic guilds prob- accurately described as a benthic invertivore (Pusey lematic (Odum 1971; Abrams 1996), a situation that is et al. 1995, 2000). In the case of both Murray cod common in studies of fish communities (Gerking 1994). Maccullochella peelii peellii and bluenose cod Mac- It may be informative to estimate trophic level (e.g. cullochella macquariensis, data is lacking. Most Corte´s 1999) or subdivide top predators into groups, striking of all is the absence of published information such as apex and top predators, if intraguild predation on the diet of M. peelii peelii Mitchell 1838. This occurs at the top of the food web to distinguish the role species supports a substantial recreational fishery, was of different predators (e.g. Rosenheim et al. 2004). once the basis of an important inland commercial In contrast to many large river systems of the world, fishery, and has high cultural and ecological signifi- the Murray- system (the largest in cance (Rowland 1989; Reid et al. 1997; Kearney &

510 doi: 10.1111/j.1600-0633.2006.00191.x Murray cod an apex predator

Kildea 2003). Furthermore, body size can be an Methods important determinant of fish community structure (Polis et al. 1989; Piet et al. 1999; conversely see Between June 1997 and February 2001, recreational Vander Zanden et al. 2000), and the massive size [up anglers in the township of Mildura (34 11¢ 142 10¢) to 1.8 m total length (TL) and 113.5 kg, Harris & provided samples and information for this study. Legal Rowland 1996] and large gape of Murray cod indicate size Murray cod (>500 mm TL) and golden perch that it may act as an apex predator within the Murray- (>300 mm TL) were collected opportunistically with Darling Basin. Specifically, Murray cod may consume anglers instructed to freeze the abdominal contents other large fishes and in particular top predatory fish from specimens and record information on the TL species. (mm) and weight of each fish (g); the time, date and To determine if Murray cod is an apex predator location of capture; the bait used; and to make (cf. Kearney & Kildea 2003) its gut contents was additional comments as required. The origin of compared with that of the other common top predator samples was then categorised according to functional golden perch M. ambigua ambigua Richardson 1845. reaches of river following Jacobs (1990; specifically Prey of length >150 mm TL were selected as a key Fig. 3.2). indication of apex predation. This threshold length Most samples of Murray cod (N ¼ 32) and golden was selected a priori because the fish community of perch (N ¼ 45) were sourced from weir pools of the the Murray-Darling Basin consists mostly of small Murray River between Loch 7 and Euston and a small native species with a typical adult size of less than number of samples (Murray cod N ¼ 8, golden perch 100 mm TL and a maximum adult size of less than N ¼ 7) were sourced from much further (>350 km) 150 mm TL (see McDowall 1996; Schiller & Harris upstream between Echuca and Lake Mulwala and 2001). Whilst these smaller species are clearly prey including the Mulwala Channel (Fig. 1; Appendixes 1 for some predatory fishes (Davis 1977; Battaglene and 2). All fish were collected during daylight hours 1991) the consumption of larger fishes remains (Appendixes 1 and 2), reflecting angler activity. In this anecdotal (e.g. Harris & Rowland 1996) and study Murray cod were collected by fishing with lures evidence of such behaviour would discern apex (60%) bait (37.5%), and by hand (2.5%; Appendix 1). predation. All golden perch were caught by fishing with bait

Fig. 1. Localities along the Murray River from where samples were collected in this study.

511 Ebner

(Appendix 2). Small sample sizes within seasons of each prey type was expressed as a percentage of precluded investigation of seasonal patterns in diet. the total weight of stomach contents in the sample. Morphological features relevant to pursuit, capture or digestion of prey by Murray cod and golden perch Results were recorded from a subsample of specimens caught by anglers and additional specimens collected during There was little overlap in the size of individuals of the other scientific studies. These features included gen- two species (Murray cod and golden perch) used in eral body and fin shape, TL (mm), standard length this study. One golden perch of 280 mm TL was (SL, mm), position and type of dentition in the mouth, slightly below the minimum legal length for recre- mouth gape (mm), number of pyloric caeca and ational angling in NSW waters but was retained after alimentary tract length (ATL, mm). Mouth gape of receiving a fatal injury whilst the angler was removing specimens was measured according to the procedure the hook. Eighty-one percent and 13% of golden perch of Pusey & Bradshaw (1986) except that fish were were of the 300–399 mm and the 400–499 mm length dead and accuracy was only to the nearest 1 mm from class (based on TL) and the two largest individuals measurement of individuals greater than 100 mm TL. were both 520 mm TL. Forty-nine percent of the Fingerlings of both species were used specifically to Murray cod sample (N ¼ 19/39) was of the 500– obtain SL, TL and gape measurements (to the nearest 599 mm length class, with a further 26%, 13% and 8% 0.05 mm) to establish an accurate plot of the length– of the 600–699, 700–799 and 800–899 mm, length gape relationship. Relative gut index (RGI) provides classes respectively. Two much larger individuals an indication of the trophic position of a species (1020 and 1250 mm TL) were also collected. (Kapoor et al. 1975) and was calculated as: RGI ¼ ATL=SL: Predator morphology Intestinal and stomach contents were examined to The food procurement and processing morphology of distinguish individual prey items and parasites. Prey both species was consistent with that of a predatory fishes were identified with the aid of McDowall fish (Table 1; see Kapoor et al. 1975; Hyatt 1979; (1996) and, in some cases, scales and vertebral Fange & Grove 1979; Gerking 1994). The body shape elements were compared with material of known of Murray cod was deep and rounded, particularly in origin. Decapods were identified with the aid of the case of larger specimens. Golden perch were also Horwitz (1995), Jones & Morgan (1994) and Geddes deep bodied but distinctly laterally compressed in (1990). Collections of whole specimens were used to body shape. Both species possessed a short and thick establish relationships between key structures and the caudal peduncle and a rounded caudal fin. This length and weight of common prey items (freshwater morphology enables short-burst swimming suitable Macrobrachium australiense, yabby for an ambush or stalking mode of predation, rather destructor, carp Cyprinus carpio, bony herring than one of a prolonged chasing or active mode of Nematalosa erebi). Prey length was measured pursuit (Pauly 1989; Gerking 1994). directly in the case of whole prey [TL of fish, and In both species the stomach was large, supporting from posterior level of orbit to the posterior edge of four pyloric caeca at the gastrointestinal junction in the telson (OTL) of decapods]. Where incomplete Murray cod and four to thirteen pyloric caeca in golden prey items were present, it was assumed that prey perch. The alimentary tract was short and therefore had been ingested as a whole (cf. Hyatt 1979) and typical of carnivores (Kapoor et al. 1975) in golden had been partly digested. Consequently, prey length perch (RGI ¼ 0.6–1.2) as was reported by Barlow et al. was derived from length relationships with consistent (1987) and Murray cod (RGI ¼ 0.5–1.0). Fat deposits morphological structures (such as carapace length of were often present on the walls of the peritoneal parastacids, vertebral column length of fishes). cavity and amongst the viscera in both species. Thawed stomach contents were also divided into prey type and weighed to the nearest 0.1 g. Dietary Table 1. Ecomorphological features of Maccullochella peelii and Macquaria items present in the intestinal contents were recorded ambigua characteristic of carnivores and particularly ambush predators. and used in analysis. Intestinal contents (usually a mucous-like substance) were not weighed or included M. peelii M. ambigua in the analysis. Diet was assessed by the numerical Body shape Rounded Laterally compressed method (Pillay 1952) where individual prey items Caudal peduncle Thick Thick were counted, the frequency of occurrence method Caudal fin Rounded Rounded where the number of individuals in the sample that Teeth Villiform Villiform had preyed upon each prey type was expressed as a Number of pyloric caeca 4 (N ¼ 32) 4–13 (N ¼ 45) percentage, and by per cent weight where the weight Relative gut index 0.5–1.0 (N ¼ 40) 0.6–1.2 (N ¼ 36)

512 Murray cod an apex predator

Table 2. A comparison of the stomach contents of Maccullochella peelii and Macquaria ambigua expressed in terms of per cent frequency of occurrence (%FO), per cent numerical count (%N) and per cent weight (%W).

M. peelii M. ambigua (N ¼ 39) (N ¼ 52)

%FO %N %W %FO %N %W

Fish 44 50 90.4 6 2 16.0 Decapods 23 48 9.3 73 97 83.9 Insects 0 0 0.0 4 1 0.1 Gastropods 3 2 0.3 0 0 0.0 Empty 31 25 Total number of prey items 44 205 Number of empty stomachs 11 13 Total prey weight (g) 681.3 102.8

Table 3. A taxonomic breakdown of the alimentary contents of Macculloch- ella peelii and Macquaria. ambigua expressed in terms of per cent frequency of occurrence (%FO) and per cent numerical count (%N). Fig. 2. The relationship between mouth size and body length in Maccullochella peelii and Macquaria ambigua. The legal size of %N %FO each species relating to gape is represented as a dotted line. M. peelii M. ambigua M. peelii M. ambigua A comparison of gape size at length (Fig. 2) Teleostei suggests that the gape increases with length at a Cyprinus carpio 23.8 0.4 35 2 Unid. Cyprinidae 3.2 0.0 5 0 slightly faster rate in Murray cod Nematalosa erebi 7.9 0.4 8 2 2 (y ¼ 0.1306x + 0.46; r ¼ 0.98) than golden perch Bidyanus bidyanus 1.6 0.0 3 0 (y ¼ 0.1079x + 1.2783; r2 ¼ 0.98). Note that this Macquaria ambigua 0.0 0.4 0 2 comparison is based on two samples that are not Unid. fish 7.9 2.4 13 8 Total Teleostei 44.4 3.7 59 10 normally distributed and with heterogenous variances. Murray cod grows to significantly greater TL and Macrobrachium 39.7 78.4 31 77 consequently attains much greater maximum mouth Paratya 0.0 1.2 0 2 Unid. 0.0 5.7 0 2 size than golden perch (Fig. 2). Observations of Cherax 11.1 7.8 15 23 villiform teeth on the dentary, premaxilla, vomer and 3.2 0.0 5 0 pharyngeals in both species are indicative of a Unid. 0.0 0.8 0 4 predatory feeding mode; and were consistent with Total Decapoda 54.0 93.9 39 90 Mollusca previous and more detailed investigations of per- Unid. terrestrial gastropod 1.6 0.0 3 0 cichthyid morphology (Berra & Weatherley 1972; Insecta MacDonald 1978; Barlow et al. 1987). Corixidae 0.0 0.4 0 2 Diptera (flying) 0.0 0.8 0 4 Diptera (larval) 0.0 0.8 0 2 Gut contents Unid. Insecta 0.0 0.4 0 2 Total Insecta 0.0 2.4 0 6 The stomach contents of 39 Murray cod (Table 2) Total number of prey items 63 245 show that fish was the dominant prey and decapods Incidental material Crustacea were of secondary importance based on frequency of Austroargathona 13 10 occurrence and weight. Numerically both fish and Sediment 3 0 decapods were the most common prey in the stomach Wood fragments 3 4 (Table 2) and intestine of Murray cod (Table 3). In Terrestrial leaf fragment 3 2 Filamentous algae 0 2 contrast, decapod prey dominated the stomach and Human hair follicle 3 0 intestinal contents of 52 golden perch (Tables 2 and 3). Sample size 39 52 39 52 In this study, Murray cod consumed three identifi- Empty alimentary tracts 11 13 3 5 able species of fishes, carp Cyprinus carpio, bony herring N. erebi and silver perch Bidyanus bidyanus. comparison, golden perch also consumed three iden- In particular, Murray cod predation on C. carpio was tifiable species of fishes, C. carpio, N. erebi and relatively common with 35% of Murray cod samples golden perch, though fish occurred infrequently in the containing C. carpio. There was only one record of B. diet. In terms of decapods, freshwater prawn Mac- bidyanus in the alimentary tract of Murray cod. In robrachium australiense were frequently consumed,

513 Ebner and yabby Cherax destructor were moderately com- mon in the diet of both predators. Murray River crayfish Euastacus armatus was recorded from 5% of Murray cod, and was only recorded from samples derived from the Murray River within the Barmah Forest (upstream of Echuca). Six percent of golden perch contained insects and a single terrestrial snail was present in a Murray cod sample. A total of nine ectoparasitic isopods Austroargathona sp. found in the alimentary tracts of five golden perch were most likely consumed incidentally in their capacity as an external parasite on M. australiense. The mechanism by which a human hair follicle, 28 cm in length, came to reside within a substantial length of the intestine of an individual Murray cod is unknown. However it must have been ingested at least hours prior to capture.

Number of prey per sample The number of prey present in the stomachs of Murray cod and golden perch differed noticeably between the two species (Fig. 3). Seventy-nine percent of Murray cod stomachs contained one prey item or less, with five as the maximum number of prey recorded from a stomach (Fig. 3). In contrast, less than 45% of golden Fig. 4. Length of prey consumed by Maccullochella peelii and perch stomachs contained one prey item or less and 21 Macquaria ambigua. Length (mm; total length of fish, OTL of was the maximum number of prey recorded from a decapods, maximum dimension of other prey) measured directly or stomach. Twenty-five percent of golden perch stom- reconstructed from partial prey items present in the alimentary tract. achs contained more than the maximum number of prey items recorded in a Murray cod stomach. These much larger prey (Fig. 4). Golden perch preyed incidences of higher prey counts (more than five prey exclusively on dietary items of less than 100 mm in per stomach) coincided with predation upon Paratya length, and most of these measurable items were or small M. australiense. decapods (Macrobrachium, Paratya, Cherax). Many of these items were small or (Mac- robrachium or occasionally Paratya) often less than Prey size 30 mm OTL. Murray cod (>500 mm TL) rarely fed on Prey size also differed between Murray cod and these small though larger decapods were golden perch with the former clearly consuming the consumed (Cherax, Euastacus, adult Macrobrach- ium). Additionally, Murray cod consumed signifi- cantly larger fish prey than did golden perch. These 50 predator-specific differences in prey size were prob- M. peelii (N = 39) ably partly a function of differences in predator size 40 M. ambigua (N = 52) (see the Methods section for predator sizes). Fifteen percent of measurable fish prey items were 30 larger than the threshold used to distinguish apex predators from other top predators (i.e. >150 mm).

20 The largest teleost prey recorded was a C. carpio of at least 410 mm TL with a predigested weight estimated Frequency (%) at approximately 1 kg, from the stomach of a Murray 10 cod that was 1250 mm TL and weighed 18 kg. The terrestrial snail found in this sample may have 0 originally been the gut contents of the C. carpio. 0 5 10 15 20 Other prey of impressive size included a C. carpio of Number of prey per stomach 200 mm TL consumed by an individual of 890 mm Fig. 3. Number of prey per stomach in Maccullochella peelii and TL, and a N. erebi of 205 mm TL consumed by an Macquaria ambigua. individual of 600 mm TL. Three N. erebi of length

514 Murray cod an apex predator

192, >247 and >127 mm TL were found in the rivers of the Basin (Harris & Gehrke 1997). Presum- stomach of an individual Murray cod of 680 mm TL. ably these major shifts in prey availability have influenced the ecology of Murray cod and the structure and function of the food web in the rivers of the Parasites Murray-Darling Basin. Changes in prey availability The red-coloured parasitic nematode Eustrongylides have been found to have major impacts on carnivores spp. was observed in the intestine of 15% of Murray in terrestrial systems (Fuller & Sievert 2001). cod and 42% of golden perch, and was present in Large-scale quantitative research into the feeding samples taken from both upstream and downstream ecology of Murray cod and the more common golden locations on the Murray River (Fig. 1). Of the four perch is necessary to develop an understanding of the Murray cod specimens examined for ectoparasites role of predators in the river systems of the Murray- only one had signs of any infection. Lesions attribut- Darling Basin. This information is necessary if we are able to the parasitic copepod, Lernaea sp., were a to properly evaluate the effects of widespread harvest- marked feature over much of the external surface of an ing and stocking of these species for recreational individual (Sample No. 35; Appendix 1) that was fisheries, and ultimately to manage our river systems found close to death floating in the Murray River near in an ecologically sustainable way (Steneck 1998). Mildura. In the order of 100 lesions could be With considerable attention given to understanding the distinguished, centred on the maxilla, dentary, gill trophic effects of harvesting and stocking of predatory arches, operculum, the lateral surfaces, underside near fishes in aquatic ecosystems elsewhere (Barthelmes the anus and all fins of this individual. 1994; Gerking 1994; Kitchell et al. 1994; Steneck 1998; Morgan et al. 2004), it is surprising that similar evaluation has not been performed in the Murray- Discussion Darling Basin (e.g. Phillips 2003). This study has confirmed that Murray cod is able to Collaboration with recreational anglers included the operate as an apex predator, feeding on large fishes in use of discards from recreational catch, and proved a the Murray River. Evidence for this comes from a successful means of obtaining information on the relatively small number of samples collected from a feeding ecology of two relatively long-lived species minor proportion of the biogeographical range of (Battaglene 1991; Rowland 1998) whilst precluding Murray cod. Far more comprehensive study is the sacrificial sampling of individuals purely for required to evaluate the anecdotal reports of Murray scientific purposes. Future research aimed at model- cod feeding on large, nonpiscine prey including ling the food consumption of Murray cod should be amphibians, reptiles, birds and mammals (Cadwallader based on nonlethal radioisotope analysis and collec- 1977; Harris & Rowland 1996) and to quantify the tion of at least some dietary samples independent of role of this predator in the river ecosytems of the angling to prevent certain biases. Bias associated with Murray-Darling Basin. In this regard, the seasonal diet angling includes selection for individuals that favour of Murray cod is a prominent knowledge gap. prey akin to the bait or lure being used. In this case The preliminary indication from this study is that Murray cod were regularly caught on lure, quite often adult Murray cod rely on a few large aquatic prey on very large lures that mimic swimming fishes species. This dietary habit was suggested by Roughley (Appendix 1). In contrast, golden perch were captured (1951) and may be widespread considering the limited with small invertebrate baits and not lures (Appendix diversity of decapods and large fishes in the lowlands 2). Similar observations were made by Roughley of the Murray-Darling Basin (cf. Geddes 1990; (1951) and provide further indication that the Murray McDowall 1996) and reduced floodplain inundation cod is a higher order predator than golden perch. associated with river regulation (Walker 1986). Of Potentially more serious is the bias against satiated concern then, are the dramatic shifts in range and fish that arises when individuals are selected based on abundance of a number of aquatic prey organisms. For their levels of hunger or activity (Pennington 1985), as example Murray River crayfish E. armatus (Geddes is the case with using angling as a sampling method. 1990; Geddes et al. 1993; Horwitz 1990) and silver As a result Murray cod and golden perch feeding on perch B. bidyanus (Reid et al. 1997; Clunie & Koehn single prey items at the upper size limit of their 2001) populations have plummeted in recent decades capability would have been inadvertently excluded in and the introduced carp C. carpio has undergone a this study. Conversely, once large prey items are massive population explosion (Harris & Gehrke 1997; ingested they are more readily detected than small Koehn et al. 2000). The native fish community in the meals owing to the more rapid digestion of the latter Murray-Darling Basin is presently estimated to be at (Beyer 1998). Therefore, it is likely that this study 10% of pre-European levels (MDBC 2004) with focussed on individuals that had not fed recently or C. carpio forming 80–90% of fish biomass in some were engaged in feeding on smaller prey items and

515 Ebner were yet to become satiated. Theoretically this prob- tions (Harris 1995a; Schiller & Harris 2001; Gehrke & lem should have been minimised (at least in the case of Harris 2004) distinguish between microphagic and organisms with hard body parts) by reconstructing macrophagic carnivores. This study suggests that prey size from intestinal contents, thereby assessing division of the latter guild into ‘apex predator’ and feeding over a longer time period rather than just the ‘top predators’ may be more informative. In the rivers instantaneous picture derived from the stomach con- of the Basin, an apex predator feeds upon large fishes tents alone. However, partial prey structures that could including other macrophagic predators. In addition to be used to reliably reconstruct the size of prey were Murray cod, it is also probable that bluenose cod rarely present in the intestinal tract. M. macquariensis sometimes grow large enough It is also important to acknowledge that the Murray (Harris & Rowland 1996) to function as apex cod used in this study were not representative of the predators, whereas Tandanus tandanus (Davis 1977) true population or the recreational angler catches. and M. ambigua (Merrick & Midgley 1985; Battag- Murray cod samples were biased by not including any lene 1991; this study) are top predators in lowland specimens smaller than legal length (500 mm TL). rivers. In times of post-European settlement the alien One problem with the lack of samples from under- redfin perch Perca fluviatilis, brown trout Salmo trutta legal size Murray cod is uncertainty about whether and rainbow trout Oncorhynchus mykiss have func- their piscivorous habit develops early and whether tioned as top predators in some areas (principally in there is more overlap with golden perch of similar size the south-east) of the Basin (McDowall 1996; Gehrke (i.e. 300–500 mm TL). A bias also occurred because & Harris 2004). most anglers that supplied samples (including one There are two functional reasons for distiguishing angler that provided more than half of the Murray cod apex predators from top predators in the fish commu- samples) had a policy of returning large individuals to nity of the Basin. First, there is a direct trophic link the river either for conservation purposes and/or between the two guilds similar to occurrences in large because they disliked the taste of the flesh from older, mammal predator fauna in terrestrial systems. The fatty Murray cod (Ebner, personal observation). In apex predators can utilise top predators as a food contrast, these anglers when questioned made it resource, and suppress populations of top predators explicit that all above legal size golden perch where whereas the reverse is not the case (e.g. Ginsberg kept for human consumption. Therefore the length 2001). Adult Murray cod are capable of feeding on frequency of golden perch that were examined in this adult golden perch whereas golden perch never attain a study was probably a more representative sample of large enough size to reciprocate (although adult golden angler catch and the true adult population than was perch may consume juvenile Murray cod). Further- that of Murray cod. Importantly, the effect of not more, members of each guild are essentially incapable retaining particularly large Murray cod was probably of predating upon the adults or at least the larger adults to reduce the number of records of its very large prey. of other species within their own guild. For instance, In this study, golden perch were found to have a diet large bluenose cod M. macquariensis outgrow (Harris that was generally consistent with reports from & Rowland 1996) the mouth size of Murray cod (this elsewhere in the Murray-Darling Basin (Cadwallader study). 1977; Battaglene 1991), the Lake Eyre Basin and the Second, apex predators are capable of exploiting Fitzroy River catchment (Merrick & Midgley 1985; other groups of prey that are inaccessible to the top Ebner, unpublished data). Collectively these studies predators owing to gape limitation, since in aquatic demonstrate that golden perch generally feed on prey systems most predators ingest prey as a whole (Hyatt smaller than about 100 mm in length. Notably the 1979; Gehrke & Harris 2004). These prey are large analysis of 852 adult golden perch stomachs conduc- microphagic carnivores, omnivores, herbivores and ted by Battaglene (1991) revealed that the largest prey detritivores similar in size to top predators though not of item was a single N. erebi of 150 mm in length. such extreme size as apex predators. Native examples The ability of Murray cod to predate upon substan- include the microcarnivores Macqu- tially larger prey than that of golden perch is probably aria australasica and river blackfish Gadopsis mar- a function of differences in predator size. Both species moratus, the omnivore silver perch B. bidyanus and the exhibit similar gape at length relationships (Fig. 2); detritivore bony herring N. erebi (Harris 1995a; Mc however, golden perch rarely attains 600 mm TL Dowall 1996). An example of an invertebrate prey item whilst it is not unusual for anglers to catch Murray cod is the Murray River crayfish E. armatus that reaches up greater than 1 m in length near Mildura (Ebner, to 3 kg in weight (Horwitz 1990). It is also clear from personal observation). The resulting difference in this study that the alien carp C. carpio has become maximum consumable prey size has a subtle but available as food for an apex predator of the Basin. important ramification for trophic classification of the From a pest management perspective, preliminary Murray-Darling Basin fish fauna. Existing classifica- indications are that golden perch are unlikely to

516 Murray cod an apex predator be capable of consuming adult carp C. carpio. References Conversely, this study has demonstrated that adult Abrams, P.A. 1996. Dynamics and interactions in food webs C. carpio at least for a few years postmaturity, are with adaptive foragers. In: Polis, G.A. & Winemiller, K.O., vulnerable to predation by large Murray cod based eds. Food webs. New York: Chapman and Hall, pp. 113– on a length–gape relationship and gut contents. It is 121. also likely that Murray cod predation on mature Barlow, C.C., McLoughlin, R. & Bock, K. 1987. Comple- C. carpio currently occurs at a depressed level over mentary feeding habits of Golden perch Macquaria much of the Basin, as a function of depleted Murray ambigua (Richardson) (Percichthyidae) and Silver perch cod stocks (Harris & Gehrke 1997; Reid et al. 1997; Bidyanus bidyanus (Mitchell) (Teraponidae) in farm dams. Kearney & Kildea 2003), and growth overfishing Proceedings of the Linnean Society of New South Wales whereby populations consist primarily of small 109: 143–152. individuals (those below minimum legal size) Barthelmes, D. 1994. Impact of intensive fishing pressure on fish populations in lakes of Eastern Germany. In: Cowx, I.G., (Koehn and Nicol, unpublished data). The impor- ed.. Rehabilitation of freshwater fisheries. Oxford, UK: tance of this trophic pathway or scope for its Fishing News Books, pp. 69–76. manipulation as a method for controlling C. carpio Battaglene, S.C. 1991. The golden perch, Macquaria ambigua has been considered (Harris 1995b; Koehn et al. (Pisces: Percichthyidae) of Lake Keepit, NSW. M.Sc. Thesis. 2000) and remains to be thoroughly investigated. In Australia: University of New South Wales. particular, the decreased diversity of native prey Berra, T.M. & Weatherley, A.H. 1972. A systematic study of species (discussed earlier) provides opportunity for the Australian freshwater serranid fish Maccullochella. Murray cod to exert a larger per capita effect on Copeia 1: 53–64. C. carpio (see Pimm 1982). Beyer, J.E. 1998. Stochastic stomach theory of fish: an This study has used a threshold length to distinguish introduction. Ecological Modelling 114: 71–93. an apex predator from top predators, within the Cadwallader, P.L. 1977. J.O. Langtry’s 1949–50 Murray River investigations. Melbourne, Australia: Victoria Fisheries and macrophagic carnivore guild of Murray-Darling Basin Wildlife Division, Paper 13: 1–70. fishes originally proposed by Harris (1995a) and Clunie, P. & Koehn, J. 2001. Silver perch: a resource document, Schiller & Harris (2001). The distinction between Vol. 2. Melbourne, Australia: Arthur Rylah Institute for these groups is fundamental, in that certain trophic Environmental Research, Final Report for Natural Resource pathways are available to one group and not the other, Management Strategy Project R7002 to the Murray Darling as a function of predator and prey size. This Basin Commission. classification should be transferred to other macro- Corte´s, E. 1999. Standardized diet compositions and trophic fauna that feed within aquatic ecosystems of the Basin, levels of sharks. ICES Journal of Marine Science 56: 707–717. most notably avian predators. For instance, the small Crabb, P. 1997. Murray-Darling Basin resources. Canberra: cormorant species Phalacrocorax sulcirostris and Murray Darling Basin Commission. Phalacrocorax melanoleucos are top predators that Davis, T.L.O. 1977. Food habits of the freshwater catfish, Tandanus tandanus Mitchell, in the Gwydir River, Australia, feed on moderately large prey including fishes of up to and effects associated with impoundment of this river by the 180 and 160 mm in length, respectively (Miller 1979). Copeton Dam. Australian Journal of Marine and Freshwater In contrast, the great cormorant Phalacrocorax carbo Research 28: 455–465. and the pelican Pelicanus conspicallatus feed on Fange, R. & Grove, D. 1979. Digestion. In: Hoar, W.S., substantially larger fishes (Marchant & Higgins 1990) Randall, D.J. & Brett, J.R., eds. Fish physiology, Vol. VIII. functioning similar to Murray cod as apex predators in New York: American Press, pp. 161–260. rivers of the Murray-Darling Basin. Fuller, T.F. & Sievert, P.R. 2001. Carnivore demography and the consequences of changes in prey availability. In: Gittle- man, J.L., Funk, S.M., Macdonald, D. & Wayne, R.K., eds. Acknowledgements Carnivore conservation. Cambridge, UK: Cambridge Uni- I am indebted to all of the recreational anglers that provided versity Press, pp. 163–178. samples for this study, especially Roger Westgarth, the South Geddes, M. 1990. Crayfish. In: Mackay, N. & Eastburn, D., eds. Mildura R.S.L. Angling Club and the participants and The Murray. Melbourne: CSIRO Publications, pp. 302–307. organisers of the Lions Club of Merbein Incorporated ‘Fishing Geddes, M.C., Musgrove, R.J. & Campbell, N.J.H. 1993. The Bonanza’, in 2000. This research benefited from a River Basin feasibility of re-establishing the River Murray crayfish, Management Society grant, use of the Murray-Darling Fresh- Euastacus armatus, in the lower River Murray. Freshwater water Research Centre’s Lower Basin Laboratory and a Ph.D. Crayfish 9: 368–379. scholarship provided by La Trobe University and the Cooper- Gehrke, P. & Harris, J. 2004. Fish in the Darling River system. ative Research Centre for Freshwater Ecology. Mark Dunford In: Breckwoldt, R., Boden, R. & Andrew, J., eds. The assisted with the production of Fig. 1, and the manuscript was Darling, Chap. 11. Canberra: Murray Darling Basin Commis- improved by the suggestions of Lee Baumgartner, Shaun sion, pp. 260–277. Meredith, Mark Lintermans, Paul Brown and two anonymous Gerking, S.D., ed. 1994. Feeding ecology of fish. San Diego: reviewers. Academic Press.

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Appendices

Appendix 1. Information on the recreational angler collections of Maccullochella peelii used in this study. Note that a single individual (sample No. 35) was close to death and was collected by hand. Comments on the condition of this specimen are provided in the Results’ section.

Specimen No. Location Date Time (hours) Bait

1 Lake Mulwala 19 May 2000 14:15 Lure 2 Mulwala Canal 12 May 2000 15:45 Cherax destructor 3 Mulwala Canal 18 May 2000 15:30 Cherax destructor 4 Murray River, Barmah 10 August 1997 10:30 Cherax destructor 5 Murray River, Barmah 10 August 1997 11:00 Bardie grub 6 Murray River, Barmah 10 August 1997 11:15 Bardie grub 7 Murray River, Barmah 10 August 1997 11:30 Cherax destructor 8 Murray River, Echuca 31 January 1998 17:45 Bardie grub 9 Lock and Weir 11 16 March 1999 17:00 Lure 10 Lock and Weir 11 7 December 1999 08:45 Lure 11 Lock and Weir 11 16 December 1999 day Steak (cow) 12 Lock and Weir 11 30 December 2000 day Macrobrachium 13 Lock and Weir 11 30 December 2000 day Bardie grub 14 Lock and Weir 11 30 December 2000 day Bardie grub 15 Lock and Weir 11 6 January 2001 10:30 Lure 16 Lock and Weir 11 6 January 2001 11:45 Lure 17 Lock and Weir 11 10 January 2001 day Lure 18 Lock and Weir 11 11 January 2001 18:45 Lure 19 Lock and Weir 10 16 January 1999 17:00 Lure 20 Lock and Weir 10 18 January 1999 17:00 Lure 21 Lock and Weir 10 18 January 1999 18:00 Lure 22 Lock and Weir 10 19 January 1999 19:30 Lure 23 Lock and Weir 10 3 February 1999 15:00 Lure 24 Lock and Weir 10 3 February 1999 15:15 Lure 25 Lock and Weir 10 4 February 1999 14:30 Lure 26 Lock and Weir 10 4 February 1999 14:50 Lure 27 Lock and Weir 10 5 February 1999 14:00 Lure 28 Lock and Weir 10 23 March 1999 17:45 Lure 29 Lock and Weir 10 23 March 1999 18:30 Lure 30 Lock and Weir 10 5 December 1999 10:00 Lure 31 Lock and Weir 10 6 December 1999 10:00 Lure 32 Lock and Weir 10 7 May 2000 14:00 Lure 33 Lock and Weir 10 7 May 2000 14:30 Lure 34 Lock and Weir 10 7 May 2000 14:50 Lure 35* Lock and Weir 10 17 November 2000 10:00 not applicable 36 Lock and Weir 10 1 January 2001 09:05 Cherax destructor 37 Lock and Weir 10 1 January 2001 09:30 Cherax destructor 38 Lock and Weir 10 4 January 2001 07:00 Cherax destructor 39 Lock and Weir 10 4 January 2001 08:00 Cherax destructor 40 Lock and Weir 10 7 January 2001 06:30 Lure

*Obtained morphological measurements and not stomach contents information from this specimen

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Appendix 2. Information on the recreational angler collections of Macquaria ambigua used in this study.

Specimen No. Location Date Time (hours) Bait

1 Lake Mulwala 17 May 2000 14:30 Cherax destructor 2 Lake Mulwala 17 May 2000 14:35 Cherax destructor 3 Murray River, Mulwala 16 May 2000 15:00 Cherax destructor 4 Mulwala Canal 12 May 2000 16:00 Cherax destructor 5 Mulwala Canal 16 May 2000 15:35 Cherax destructor 6 Echuca (Goulbourn Road) 26 October 1997 Day Worm 7 Murray River, Echuca 8 December 1997 20:00 Worm 8 Britts Bend (Murray River) 7 June 1997 10:15 Macrobrachium 9 Britts Bend (Murray River) 7 June 1997 10:20 Macrobrachium 10 Britts Bend (Murray River) 7 June 1997 23:00 Worm 11 Britts Bend (Murray River) 7 June 1997 23:30 Macrobrachium 12 Britts Bend (Murray River) 8 June 1997 09:45 Macrobrachium 13 Britts Bend (Murray River) 8 June 1997 10:00 Worm 14 Britts Bend (Murray River) 8 June 1997 10:55 Macrobrachium and worm 15 Britts Bend (Murray River) 9 June 1997 08:00 Macrobrachium 16 Murray River, Kullkyne 16 December 1999 Day Macrobrachium 17 Lock and Weir 11 29 April 2000 17:00 Macrobrachium 18 Lock and Weir 11 29 April 2000 17:00 Macrobrachium 19 Lock and Weir 11 18 February 2001 Day Macrobrachium 20 Lock and Weir 11 18 February 2001 Day Macrobrachium 21 Lock and Weir 11 18 February 2001 Day Macrobrachium 22 Lock and Weir 11 18 February 2001 Day Macrobrachium 23 Lock and Weir 11 18 February 2001 Day Macrobrachium and worm 24 Lock and Weir 10 7 May 2000 Day Macrobrachium 25 Lock and Weir 10 7 May 2000 Day Macrobrachium 26 Lock and Weir 10 7 May 2000 Day Macrobrachium 27 Lock and Weir 10 7 May 2000 Day Macrobrachium 28 Lock and Weir 10 7 May 2000 Day Macrobrachium 29 Lock and Weir 10 7 May 2000 Day Macrobrachium 30 Lock and Weir 10 7 May 2000 14:20 Macrobrachium 31 Lock and Weir 10 7 May 2000 14:45 Macrobrachium and worm 32 Lock and Weir 10 7 May 2000 09:00 Worm 33 Lock and Weir 10 7 May 2000 14:45 Cherax destructor 34 Lock and Weir 10 7 May 2000 13:45 Macrobrachium 35 Lock and Weir 10 7 May 2000 14:00 Worm 36 Lock and Weir 10 7 May 2000 Day Macrobrachium 37 Lock and Weir 10 31 December 2000 15:30 Macrobrachium 38 Lock and Weir 9 1 April 2000 10:45 Octopus 39 Lock and Weir 9 1 April 2000 14:30 Macrobrachium 40 Lock and Weir 9 1 April 2000 14:45 Macrobrachium 41 Lock and Weir 9 1 April 2000 11:00 Macrobrachium 42 Lock and Weir 9 1 April 2000 16:35 Macrobrachium 43 Lock and Weir 9 1 April 2000 16:40 Macrobrachium 44 Lock and Weir 9 1 April 2000 16:35 Macrobrachium 45 Lock and Weir 9 1 April 2000 16:30 Macrobrachium 46 Lock and Weir 9 1 April 2000 11:00 Macrobrachium 47 Lock and Weir 9 1 April 2000 16:30 Macrobrachium 48 Lock and Weir 9 1 April 2000 10:40 Macrobrachium and worm 49 Lock and Weir 9 8 April 2000 10:10 Macrobrachium 50 Lock and Weir 9 8 April 2000 11:40 Macrobrachium 51 Lock and Weir 9 24 April 2000 11:00 Macrobrachium 52 Lock and Weir 9 24 April 2000 11:00 Macrobrachium

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