Food limited survival of larval razorback sucker, Xyrauchen texanus, in the laboratory

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1 Environmental Biology of Fishes 29: 73-78, Kluwer Academic Publishers. Printed in the Netherlands Food limited survival of larval razorback sucker, Xyrauchen texanus, in the laboratory Diana Papoulias & Wendell L. Minckley Department of Zoology, Arizona State University Tempe, AZ , U.S.A. Present address: U.S. Fish and Wildlife Service, National Fisheries Contaminant Research Center, 4200 New Haven Rd., Columbia, MO 65203, U.S.A. Received Accepted Key words: Critical period, Starvation, Mortality, Fish larvae, Catostomidae Synopsis Razorback suckers in Lake Mohave, Arizona-Nevada, are suffering recruitment failure. Concomitantly, lake zooplankton levels are low and variable. We test, under laboratory conditions, the possibility that starvation is a cause of low recruitment. Razorback sucker larvae that were starved, received food too late, or were provided with insufficient food died between 20 and 30 d after hatching. Yolk absorption was at - 8 d after hatching, the critical period during which larvae must feed or most will die lies between - 8 and 19 d, and the point of irreversible starvation for individuals is between 19 and 23 d after hatching. Results support food-related mortality as a contributor to year-class failure of razorback sucker in Lake Mohave. Introduction Starvation of larvae has long been suggested as a cause of mortality which may reduce recruitment to adult populations of fishes (Hjort 1914, 1926, Cushing 1976, Leggett 1986). Larvae are especially vulnerable when switching from endogenous (yolk) reserves to exogenous nutrition, termed the critical period by May (1974), when they must encounter and capture foods sufficient in quality and quantity to sustain life and promote growth and development. The razorback sucker, Xyrauchen texanus (Abbott), a large, endemic species of the Colorado River basin, western U.S.A., is disappearing due to chronic year-class failure (Lanigan & Tyus 1988, Minckley et al. 1990). No recruitment to known adult populations has been detected for approximately 30 years, despite extensive sampling with appropriate gear (McAda & Wydoski 1980, Minckley 1983, Tyus 1987). In Lake Mohave, Arizona- Nevada, old adults remain common (Minckley 1983, McCarthy & Minckley 1987)) and reproduce every year, but larvae disappear at an average size of 10.6mm total length (TL). These wild-caught larvae have reduced or absorbed yolksacs and their stomachs are mostly empty. Concomitantly, lake zooplankton densities tend to be low and variable (Paulson et al. 1980, Langhorst & Marsh 1986). Disappearance of larvae may be related to limited food during a critical period. The three laboratory experiments reported here were designed to assess effects of absence, delayed presentation, and variable quantities of food on larval razorback mortality and growth during and immediately following the transition from endogenous to exogenous feeding. Methods Experiments were performed at Dexter National

2 74 Fish Hatchery (NFH), New Mexico. Glass jars (3.91) containing larvae were arranged in rows in indoor raceways, with position effects minimized by a constant-temperature (18 C) water bath and uniform lighting. Continuous water flow at - 100ml min-, which maintained jars at full capacity, was provided from 2.54 cm pipes perforated above each container. Jars were tilted to facilitate outflow and screened to prevent loss of fish and food. Adult (Lake Mohave) female suckers received three intramuscular injections of 220 IU chorionic gonadotropin kg- body weight at 24h intervals (Hamman 1985) beginning 11 February About 24h after the third injection, eggs were stripped and fertilized by milt from naturally-ripened, Lake Mohave males. Fertilized eggs were incubated at 21 C in Heath@ trays (Inslee 1982). Hatching began on 18 February, and larvae first swam actively on 23 February. On 25 February, 9.6 to 10.7mm TL (Mean = (SE) mm, n = 50) larvae were stocked at 10 jar- ; studies lasted 50 days, until 16 April. We examined starvation in Experiment 1 and the pattern of razorback sucker larvae mortality over time in the total absence of food; six replications (jars) were performed. The time to irreversible starvation was measured in Experiment 2. Larvae were considered irreversibly starved when, after being without food for a predetermined period of time, death could not be prevented by offering food. The point of irreversible starvation was defined as the number of days to a cumulative larval mortality > 50%. This point was determined by delaying introduction of food to the jars containing the larvae. Seven treatments with 3 replicates (jars) were established such that individual jars of larvae were without food for 7,11,15,19,23,27 and 31 d after hatching, then offered newly-hatched brine shrimp (Artemia dim) nauplii at 3001-l for the remaining 50, 46,42, 38, 34, 30, and 26d, respectively, of the experiment. In Experiment 3, we studied the effect of ration size on mortality and growth of razorback sucker larvae. Six treatments, each replicated in 3 jars, consisted of individual jars of larvae fed brine shrimp nauplii at concentrations of 5,10, 50,100,500, and looo-. For experiments 2 and 3, the individual jars of 10 larvae were offered the predetermined numbers of live Artemia nauplii three times d- at 8 h intervals. Nauplii were from San Francisco Brand@ eggs incubated in aerated 3.91 jars at C for 36 h, by which time most had hatched. Jars were agitated and allowed to stand for 1/2h. During this time nauplii accumulated near the bottom from where they were siphoned, nearly free of egg cases, to a beaker. Densities in concentrated samples were estimated by five counts of l.oml aliquots in a Sedgewick-Rafter cell. Appropriate amounts were prepared by dilution for selected levels of feeding. Levels of food are quoted as the nominal feeding rate, e.g., a container receiving a nominal 50 nauplii 1-l feeding- (150 nauplii 1-l d-l) is quoted as 50 nauplii 1-l. Individual containers (including those not receiving food) were inspected for dead larvae and siphoned clean of accumulated materials prior to each feeding. Dead larvae were preserved in 5% buffered formalin. Not all dead larvae were recovered; some became lodged and undetected beneath screens, some were inadvertently killed by siphoning, and others may have decomposed. Such larvae were considered as mortalities. To estimate minimum prey density necessary for 50% slurvival, unaccounted mortalities were distributed over dates when known mortalities occurred according to the following formula (O Connell & Raymond 1970) : mn= d,+ (P- S- D) d,/d where m, = total dead on day n; d, = dead observed on day n; P = initial population; S = survivors; and D = dead observed on all days. All mortalities were recorded by date, and if possible, measured. Surviving larvae were preserved in 5% buffered formalin and measured at the conclusion of the experiment. Data for Experiments 2 and 3 were statistically evaluated using the Kruskal-Wallis test (p < 0.05). Means in text are followed by f one standard error.

3 75 Results Experiment 1 Median time to 50% mortality of unfed razorback sucker larvae was between 24 and 25 d post-hatching. The majority of larvae died between 20 and 30 d post-hatching. Average TL at death was 9.6 f 0.2 mm (n = 28). Experiment 2 No mortality was experienced by larvae receiving food on day seven post-hatch. Larvae that began receiving food beginning on d 11, 15, and 19 posthatch had respective mortalities of 10.0, 10.0, and 26.7%. There were no significant differences among 7, 11, 15, and 19 d (Table 1). Highest death rates occurred when larvae were deprived of food for 27 (86.7%) and 31 d (93.3%), with no statistical Table 1. Experiment 2. Comparison of percentage mortalities (top) and total length (TL; bottom) + the standard error (SE) after 50 d of life for treatments in which food was withheld from razorback sucker larvae for 7, 11, 1.5, 19,23,27, and 31 d after hatching. Differing letters in parentheses denote significant differences (p czo.05) in pairwise comparisons of treatment means. Age at initial feeding (d after hatching) Mean mortality, % f SE ( IL 13.3 (XY) (Y Number specimens Mean TL mm+se Range TL (mm) f * , A differences between the last values. As in Experiment 1, the majority died between 20 and 30 d at an average size of 9.3 f 0.1 mm TL (n = 35). Surviving larvae were larger (n = 24, mm) when fed from d 7 and smaller (n = 2, 15.1 and 16.4mm) when first fed at d 31 (Table 1). Experiment 3 Mortality was greatest and not significantly different when larvae were fed either 5 or 10 nauplii 1-l ( and 73.3 f 3.3%). Larvae fed 50, 100, 500, and 1000 nauplii 1-l all had < 20% mortality, with no significant differences among treatments (Table 2). Death rates leveled when larval mortality was sufficient to provide survivors at least 10 to 20 nauplii fish- feeding-l in the 5- and lo-nauplii 1-l treatments (Table 3). Most larval deaths were again between 20 and 30 d, at a mean of mm TL (n = 25). Larvae surviving 50 d (Table 4) on rations of 5 and 10 nauplii 1-l did not differ significantly in TL. Those larvae receiving 100 nauplii 1-l were significantly larger than those in the 10 nauplii 1-l treatment, but significantly smaller than larvae receiving 500 and 1000 nauplii 1-l. Threshold density of prey, beyond which mortalities did not decrease significantly, was 50 nauplii 1-l (Table 2). The minimum densities yielding < 50% mortality were between 10 and 50 nauplii 1-l. At 50 nauplii l-l, each larva was exposed to - 20 nauplii 3 times d-l. In treatments receiving 5 and 10 nauplii l-, mortality during the experiment Table2. Experiment 3. Percentage mortality of razorback sucker larvae fed 5,10,50,100,500, and 1000 brine shrimp nauplii 1-t three times d- f standard error (SE). Differing letters in parentheses denote significant differences (p < 0.05) in pairwise comparisons of treatment means. Nauplii I- Mean mortality, % + SE ) IL 3.3 (x) f 6.6 (Y) zk 5.8 (Y) (Y) * 5.8 (Y)

4 76 resulted in a range of 10 to - 20 nauplii fish- at each of 3 feedings at termination of the experiment (Table 3). Survivors grew nearly as large as those receiving - 50 nauplii 1-l from the onset of the experiment (Table 4) indicating that 30 to 60 nauplii fish- d-l was near a minimum required to survive the critical period. Discussion Razorback sucker larvae that were starved, received food too late, or were fed an insufficient quantity usually died between 20 and 30d after hatching (Fig. 1, 2). Exact time of yolk absorption was not recorded in these experiments, but was estimated at 8 d post-hatch based on observed presence or absence of yolk in dead larvae and from Minckley & Gustafson (1982). Larvae persisted with < 30% losses for 11 d after yolk absorption, but mortality increased to > 50% after 15 d even though food was presented (Fig. 1). The critical period at 18 C, during which larvae must find and consume suitable food or die, therefore lies between - 8 and 19 d after hatching, and the point of no return, when starvation is irreversible (Werner & Blaxter 1980, Powell & Chester 1985), lies between 19 and 23 d. Fish larvae utilize energy from foods directly for growth (Blaxter 1969). Rapid growth may make them less vulnerable to predation (Cushing 1976) Table 3. Experiment 3. Number of food organisms per individual razorback sucker larva at beginning and end of 50 d feeding experiments f standard error (SE). Differing letters in parentheses denote significant differences (p < 0.05) in pairwise comparisons of treatment means. Nauplii I- Nauplii larva- (beginning) Mean+ SE Range nauplii larva- number of (end) nauplii and environmental hazards, but more dependent on reliable exogenous foods due to minimal energy reserves (O Connell & Raymond 1970, Taylor & Freeberg 1984). Razorback sucker larvae starved for different periods, but surviving to take advantage of food when finally offered, grew reasonably well compared to those fed from d 1. No specific data are available on sizes at which razorback suckers hatch in Lake Mohave, nor on the efficiency of yolk utilization, nor rates of growth at ambient temperatures. Razorback sucker in Lake Mohave have been observed spawning from early January through April with hatching occurring from February to May (Langhorst & Marsh 1986). Temperature of Lake Mohave during the period when the eggs are incubating tends to be lower than the incubation temperature for the eggs of the larvae used in our experiments (9 to 15 C vs. 21 C). However, Marsh (1985) found that although razorback sucker embryos hatched almost two-thirds as slowly at 15 as 20 C (5.5 vs. 8.5 d), TL at swim-up was not significantly different (8.5 vs. 8.4mm). Temperature in Lake Mohave during the period after hatching (ls C-17 C; Langhorst & Marsh 1986) more closely parallels the temperature in our experiments (18 C). Larvae captured from Lake Mohave proper average 10.6mm TL, while the largest larva caught measured 12.2 mm TL (Marsh & Langhorst 1988). No razorback suckers larger than this have been caught except for those in the year age-class. Those larvae which have been taken have reduced Table 4. Experiment 3. Total length (TL) f standard error (SE) of surviving razorback sucker larvae fed 5,10,50,100,500, and 1000 nauplii 1-l three times d-r. Differing letters in parentheses denote significant differences (p < 0.05) in pahwise comparisons of treatment means. Nauplii 1-l Number Mean TL Range specimens (mm) rf: SE TL (mm) f 3.2 (x) 9% f 0.5 (x) f 2.0 (x) (x) (x) f 0.3 (x) (y) 43% 55.7 loo (y) (z) I!X 0.6 (z) k 28.2 (w) f 0.7 (z)

5 4 80 k k 8 $4 '3.- i3 54 E2 ZO $4 f2 2O L 0 c k c 20 t a Days post-hatching Fig. 2. Temporal distributions of mortalities in variable-ration experiments (B-E) compared with that of starved razorback sucker larvae (A). The continuous vertical line at d 8 indicates the approximate time of yolk absorption; treatment ration and percentage mortality are in the upper right comer. Mortalities for rations of 500 and 1000 nauplii 1-l are not presented since no dead fish were recovered. t-4.../.../...i J OH Days post-hatching Fig. 1. Temporal distribution of mortalities in delayed feeding experiments (B-H) compared with that of starved razorback sucker larvae (A). The continuous vertical line at d 8 indicates the approximate time of yolk absorption; arrows indicate days on which each set of larvae (B-H) were first provided food. Percentage mortality is in the upper right comer. or completely-absorbed yolksacs, and predominately empty stomachs (Marsh & Langhorst 1988). In addition, reported average densities of zooplankton in areas of Lake Mohave proper where larvae have been captured vary from 1.5 to 26.3 organisms 1-l (Marsh & Langhorst 1988, Paulson unpublished data). Furthermore, only a portion of this zooplankton biomass is presumably available to the larvae. Marsh & Langhorst (1988) reported that the preferred foods of razorback larvae in Lake Mohave were cladocerans and that these comprised nearly 64% of total zooplankton density. Our results suggest that wild-caught larvae from Lake Mohave are in transition from dependence on endogenous to exogenous foods, and therefore in the critical period. In our experiments, starvation killed most d old larvae. Experimental larvae at death measured only slightly less ( mm TL) than the average wild-caught larva (10.6mm TL) as estimated by Marsh & Langhorst (1988), at most, a few weeks old. However, some larvae in our 50 d experiments that had received a sub-optimal ration of brine shrimp were nearly half the size of those receiving excess nauplii indicating that age may not be reliably predicted from size when food

6 78 is limiting. Finally, lake zooplankton densities, especially in the lower end of the range, may cause > 50% of the larvae to die of starvation. Foodrelated mortality may thus contribute to the consistent absence of recruitment to the adult razorback sucker population in Lake Mohave. Acknowledgements The authors thank Buddy Jensen and his staff at the Dexter National Fish Hatchery for their assistance and the use of hatchery facilities. Environmental Biology of Fishes reviewers are also thanked for improving the manuscript. This research was funded by the U.S. Fish and Wildlife Service, Office of Endangered Species under contracts and References Blaxter, J.H.S Development: eggs and larvae. pp In: W.S. Hoar & D.J. RandalI (ed.) Fish Physiology, Volume 3, Academic Press, New York. Cushing, D.H Biology of fishes in the pelagiccommunity. pp In: D.H. Cushing & J.H. Walsh (ed.) The Ecology of the Seas, W.B. Saunders, Philadelphia. Hamman, R.L Induced spawning of hatchery-reared razorback sucker. Progr. Fish-Cult 47: Hjort, J Fluctuations in the great fisheries of northern Europe viewed in the light of biological research. Rapp. P.-v. Reun. Cons. Perm. int. Explor. Mer 20: l-228. Hjort, J Fluctuations in the year class of important food fishes. J. Cons. Perm. int. Explor. Mer 1: Inslee, T.D Spawning and hatching of the razorback sucker (Xyruuchen rexanus). Proceedings of the Annual Conference of the Western Association of Fish and Wildlife Agencies, Las Vegas, Nevada, July 1985,1982: (Abstract). Langhorst, D.R. & P.C. Marsh Early life history of razorback sucker in Lake Mohave. Final Report, U.S. Bureau of Reclamation, Lower Colorado Region Contract 5- PG , Arizona State University, Tempe. 24 pp. Lanigan, S.H. & H.M. Tyus Population size and status of the razorback sucker in the Green River basin, Utah and Colorado. North Amer. J. Fish. Manag. 4 (in press). Leggett, W.C The dependence of fish larval survival on food and predator densities. pp In: S. Skreslet (ed.) The Role of Freshwater Outflow in Coastal Marine Ecosystems, Springer-Verlag, New York. Marsh, P.C Effect of incubation temperature on survival of embryos of native Colorado River fishes. Southwest. Nat. 30: Marsh, P.C. & D.R. Langhorst Feeding and fate of wild larval razorback suckers. Env. Biol. Fish. 21: May, R.C Larva1 mortality in marine fishes and the critical period concept. pp In: J.H.S. Blaxter (ed.) The Early Life History of Fish, Springer-Verlag, Berlin. McAda, C.W. & R.S. Wydoski The razorback sucker, Xyrauchen texanus, in the Upper Colorado River Basin, United States Fish and Wildlife Service, Technical Paper 99: McCarthy, M.W. & W.L. Minckley Age estimation for razorback sucker (Pisces: Catostomidae) from Lake Mohave, Arizona and Nevada. J. Ariz.-Nev. Acad. Sci. 21: Minckley, W.L Status of the razorback sucker, Xymuthen texanus (Abbott), in the lower Colorado River basin. Southwest. Nat. 28: Minckley, W.L. & E.S. Gustafson Early development of the razorback sucker, Xyruuchen texanus (Abbott). Great Basin Nat. 42: Minckley, W.L., P.C. Marsh & J.E. Brooks Management toward recovery of razorback sucker. In: W.L. Minckley & J.E. Deacon (ed.) Battle Against Extinction: 20 Years of Native Fish Management in the American West, University of Arizona Press, Tucson. (in press). O Connell, C.P. & L.P. Raymond The effect of food density on survival and growth of early and post yolksac larvae of the northern anchovy (Engruulis mordux) in the laboratory. J. Exp. Mar. Biol. Ecol. 5: Paulson, L.J., J.R. Baker & J.E. Deacon The limnological status of Lake Mead and Lake Mohave under present and future powerplant operations of Hoover Dam. Final Report, U.S. Bureau of Reclamation, Lower Colorado River Region Contract (Technical Report 1, Lake Mead Limnological Research Center), University of Nevada, Las Vegas, Las Vegas. 229 pp. Powell, A.B. & A.J. Chester Morphometric indices of nutritional condition and sensitivity to starvation of spot larvae. Trans. Amer. Fish. Sot. 114: Taylor, W.W. & M.H. Freeberg Effect of food abundance on larva1 lake whitefish, Coregonus clupeuformis Mitchill, growth and survival. J. Fish Biol. 25: Tyus, H.M Distribution, reproduction, and habitat useof the razorback sucker in the Green River, Utah, Trans. Amer. Fish. Sot. 116: Werner, R.G. & J.H.S. Blaxter Growth and survival of larval herring in relation to prey density. Can. J. Fish. Aquat. Sci. 37: