Effects of subcutaneous transmitter implants on behavior, growth, energetics, and survival of Common Loon chicks

Transcription

1 J. Field Ornithol. 74(2): , 2003 Effects of subcutaneous transmitter implants on behavior, growth, energetics, and survival of Common Loon chicks Kevin P. Kenow, 1,5 Michael W. Meyer, 2 Francois Fournier, 3,6 William H. Karasov, 3 Abdulaziz Elfessi, 4 and Steve Gutreuter 1 1 U.S. Geological Survey, Upper Midwest Environmental Sciences Center, 2630 Fanta Reed Road, La Crosse, Wisconsin USA 2 Wisconsin Department of Natural Resources, 107 Sutliff Avenue, Rhinelander, Wisconsin USA 3 Department of Wildlife Ecology, 226 Russell Labs, University of Wisconsin-Madison, Madison, Wisconsin USA 4 Department of Mathematics, University of Wisconsin-La Crosse, La Crosse, Wisconsin USA Received 2 May 2002; accepted 16 September 2002 ABSTRACT. High rates of Common Loon (Gavia immer) chick mortality have been documented in Wisconsin, especially on acidic lakes, but causes and timing of chick mortality are poorly understood. We modified and evaluated a subcutaneous transmitter implant technique for Common Loon chicks using wild and captive reared chicks. Results indicated that behavior, growth, energy expenditure, and survival did not differ significantly between chicks marked with miniature transmitters (mass 0.76 g, representing 0.8% of body mass at hatching) and unmarked chicks. SINOPSIS. Efecto de transmisores implantados subcutaniamente en la conducta, crecimiento energética y supervivencia de polluelos de Gavia immer Se han documentado, particularmente en Wisconsin, altas tasas de mortalidad en polluelos de Gavia immer particular en lagos asirificados. Sin embargo, las causas y el período de mortalidad no se entienden claramente. Evaluamos un radiotransmisor modificado implantado subcutaniamente en polluelos cautivos y silvestres de la especie antes mencionada (de masa de 0.76 g, representado 0.8% de la masa corporal al nacer). Los resultados indican que la conducta, crecimiento, gasto energético y supervivencia no varió significativamente entre los polluelos con radiotransmisores y un grupo control. Key words: Common Loon, effects, Gavia immer, radiomarking, surgical implant, telemetry, transmitter implant Annual recruitment rates of juvenile Common Loons (Gavia immer) in Wisconsin were low (average 0.60 chicks fledged per breeding pair) in lakes studied by the Wisconsin Department of Natural Resources (WDNR) from 1992 to 2000 (M. Meyer, unpubl. data). Despite inconsistencies in methods used, these rates are among the lowest productivity estimates reported for Common Loon populations (McIntyre 1988). Common Loon productivity is lower on acidic lakes than on lakes with neutral ph. Loons nesting on acidic lakes are exposed to elevated levels of dietary mercury (Meyer et al. 1995). Over an 8-yr period 5 Corresponding author. kevin kenow@ usgs.gov 6 Current address: Département de biologie, Université de Moncton, Moncton, New Brunswick E1A 3E9, Canada. ( ), loon chick fledging rates on low ph lakes were significantly lower than on neutral ph lakes (M. Meyer, unpubl. data). Elevated mercury exposure and depressed prey (fish) abundance have been implicated, but the causes and timing of chick mortality are poorly understood. Traditional observation studies have provided only limited information on loon chick productivity and have been ineffective in identifying the specific causes of mortality. Management efforts to improve productivity and survival of Common Loons cannot be effectively implemented until factors contributing to mortality are better understood. Recent advances in transmitter attachment techniques (Korschgen et al. 1996a) have allowed biologists to obtain data on movements, daily survival rates, and causes of mortality of ducklings (Korschgen et al. 1996b) using subcutaneously implanted 179

2 180 K. P. Kenow et al. J. Field Ornithol. Spring 2003 transmitters. The objectives of our study were to develop a radio-marking technique to determine the causes and timing of loon chick mortality from hatching to fledging, and evaluate the effects of the radio-marking technique on behavior, growth, energy expenditure, and survival of the chicks. METHODS This study was conducted during 1998 in conjunction with ongoing studies of Common Loon productivity. The study area encompassed lakes over a 4400 km 2 area in Oneida, Vilas, Forest, and Iron counties in northern Wisconsin. Because loon productivity appears related to lake ph, study lakes were selected from among lakes that were either low-ph ( ) or intermediate/neutral-ph ( 6.0). Some techniques were developed during pilot studies in Egg collection and incubation. Shoreline areas of lakes within the study area were searched for loon nests following the methods of Titus and VanDruff (1981). Frequent visits to loon territories allowed us to determine the date of nest initiation (first egg laid) within 2 days. Each egg was assessed for viability (Mineau and Pedrosa 1986), measured (length and width) with digital calipers, weighed, and marked with a unique number using a Sharpie permanent marker. We collected one egg from each nest following d of incubation. The collected egg was randomly selected from among the first or second egg laid. Water-filled (37 C) plastic eggs (83 57 mm, 125 g) were painted to match the color of Common Loon eggs and substituted in place of the eggs removed from the nest. Collected eggs were transported in insulated coolers heated (37 C) with water bottles or in temperature-controlled coolers. Disturbance of the nest and surrounding vegetation and the duration of the visit were kept to a minimum. Eggs were hatched in incubators and periodically checked for viability. Target incubator conditions were 37.5 C dry-bulb and C wet-bulb (RH 56 60%). Pipped eggs were transferred to a hatcher. Target hatcher conditions were 37.2 C dry-bulb and C wet-bulb (RH 76 82%). Radiomarking. Following hatching we weighed each chick, measured body length (from the anterior tip of the bill to the posterior tip of the pygostyle of the outstretched chick), attached a web-tag (Haramis and Nice 1980), and held the chicks in a brooder until they were released. The chicks were radiomarked with a miniature radiotransmitter (model BD-2T, Holohil Systems, Ltd.) following procedures adapted from Korschgen et al. (1996a). Transmitters had an average mass of 0.76 g, measured about mm, and had a life expectancy of 21 d. The transmitters were implanted subcutaneously in the chicks within a few hours of hatching. Handling and care of the chicks and surgical techniques were approved by the Animal Care and Use Committee of the Upper Midwest Environmental Sciences Center. Transmitters were implanted while the chicks were under a general anesthetic. Transmitters were disinfected in a 10% bleach solution for about 30 min, rinsed with distilled water, and stored in chlorohexidine diacetate solution until surgery. Anesthesia was induced by passing a concentration of 3.0 to 5.0% isoflurane in oxygen at a flow rate of about 1.25 l/min using an out-of-circuit, agent-specific vaporizer and a mask. A surgical level of anesthesia was maintained with a % concentration of isoflurane in oxygen. Each loon was placed on its ventral surface and held with its legs straight out. When the loon lacked eye or toe-pinch reflexes, the surgical site was prepared immediately posterior to the nape along the dorsal midline of the interscapular region. Adjacent down was wetted to expose the incision site and the site was disinfected with 1% povidone-iodine solution. An 8 10 mm incision was made immediately posterior to the nape along the dorsal midline of the interscapular region. A 2.80-mm OD (2.00-mm ID, 80 mm length) cannula (distal end open with smooth edges, modified by grinding) was inserted into the incision and used to separate skin from underlying muscle posteriorly from the incision, forming a pocket between the skin and muscle for placement of the transmitter. The pocket was extended posteriorly to the synsacrum. The distal end of the cannula was placed in position at the point where the antenna was to exit, and a stainless steel tube with sharpened end (1.47 mm OD, 0.90 mm ID, 100 mm length) was fed posteriorly through the proximal end of the cannula

3 Vol. 74, No. 2 Radio Transmitters and Common Loons 181 until it punctured the skin. The cannula was removed by backing it out over the stainless steel tube. The transmitter antenna (0.63 mm diameter with 1.40 mm diameter base) was inserted into the anterior end of the sharpened tube until it appeared at the posterior end of the tube. The tube was removed from the chick through the antenna exit site. The transmitter was pushed through the incision into the pocket and placed completely posterior to the incision ( 4 mm) such that it did not place pressure on the incision after it was closed. The incision was inspected and closed with two mattress stitches per Korschgen et al. (1996a). After surgery, pure oxygen was administered until the loon s respiratory rate returned to normal. We physically restrained the loon until it demonstrated control of head and neck and was able to assume an alert posture. The implant technique reflected pilot work we conducted in 1997, when we radio-marked eight loon chicks using a similar, but larger (1.5 g, mm, 35-d life) transmitter and released the chicks to their natal nests. Mortality among those chicks was high (20-d survival rate of 0.25), with most deaths occurring within 1.4 d. Those deaths suggested to us that the implant procedure was disrupting the waterproofing of the chick s down. Transmitter retention was also problematic as all three of the chicks that survived past 15 d lost their transmitters within 6 11 d after release. Based on an examination of chicks that had lost their transmitters, it appeared that migration of the transmitter due to rapid body growth (10-fold increase in mass in 20 d), coupled with pressure necrosis of overlying tissue, contributed to the transmitter loss. In 1998, we used a smaller transmitter and modified the implant technique to keep the surgical procedure as dry as possible and using only a few drops of saline solution to part down at the implant site and then applying a small amount of 1% povidone-iodine solution with a Q-tip along the incision site. With these modifications, the chick s down was left dry and fluffy at the end of the surgery except for the immediate area of the incision site. Chick release. Radio-marked loon chicks were returned to natal nests as soon as possible after hatching to enhance imprinting on the parents (Korschgen et al. 1996b). To restrain chicks in the nest until the parent returned, we placed the radio-marked chick and any sibling chicks in a paper envelope made of a single hand towel (finished size about mm). The top of the envelope was stapled closed. The envelope was easily ripped open by the chicks, especially after it had been wetted by moisture from the nest substrate or returning adult. We monitored the nest from a distance with binoculars or a spotting scope to confirm that nesting adults accepted the chick. Captive rearing. Six Common Loon chicks were reared in captivity following the techniques of J. Pichner (pers. comm.), Pichner and DonCarlos (1986), and Barr (1996). These chicks were artificially incubated and hatched. Three of the chicks, selected at random, were radio-marked. Chicks were held indoors in m raceways that contained about 25 cm of water, a resting platform, and a brooder light until they were about 30 d old. Room lighting was maintained at an approximate 16L:8D light cycle. Chicks were transferred to 48-m 2 outdoor ponds flooded to a depth of approximately 0.6 m and equipped with a resting platform and brooder. A constant supply of well water (approximately 12 C) was supplied to the raceways and outdoor ponds. Chicks were fed fish (primarily rainbow trout [Salmo gairdneri]) ad libitum. The size of fish provided was increased gradually from an average of 1.0 g on day 1 to 20.0 g by week 8. The diet was supplemented with thiamine and multivitamins. Records detailing thermal environment, body mass, condition, development, food consumption, and behavioral development were maintained daily for each individual. Behavior evaluation. Observations of radio-marked and unmarked chicks were conducted using an instantaneous sampling procedure (Altmann 1974). Observations of sibling chicks in the wild and among broodmates reared in captivity were made simultaneously. Behavior of the wild chicks was recorded at 30- s intervals for a 1-h period for 1 to 3 d after release. Behavior of captive-reared chicks was recorded on 15 d during the first 22 d after hatching. Chick behavior was classified according to Evers (1994) as resting, feeding, locomotion, brooding, or preening. Behavior of captive birds fell primarily in the categories of resting, locomotion, or preening. We also characterized the spatial relationship of wild-reared chicks to the adult as on adult s back, under

4 182 K. P. Kenow et al. J. Field Ornithol. Spring 2003 adult s wing, on water 1 m from adult, on water 1 m from adult, or on nest. For captive chicks, we recorded whether the chick was on the brooding platform or in the water at each observation. We treated behavioral observations as compositional data (Aebischer et al. 1993) and conducted multivariate analysis of variance (MANOVA) on additive log ratio-transformed data to test for effects of radio-marking on behavior of radio-marked and unmarked chicks. Determination of daily energy expenditure and growth. Daily energy expenditure of radio-marked and unmarked loon chicks was determined using the doubly-labeled water (DLW) method (Lifson and McClintock 1966; Nagy 1980). We increased background enrichments of 18 O and deuterium in wild and captive chicks via injection at 10, 21, and 35 d. CO 2 production was calculated using the change in 18 O and deuterium enrichment between blood samples collected at the time of enrichment and 2 to 3 d later. Energy expenditure (kj/d) was calculated from CO 2 production assuming an energetic conversion factor of 25.7 J/mL CO 2 for a fish diet (Ricklefs 1974; Nagy 1983). Wild-reared loon chicks were captured using nightlighting techniques (Evers 1993). At each capture, chicks were weighed to the nearest 0.1 g, measured to obtain indices to structural size (e.g., body length), and the transmitter site was assessed for external evidence of histological reactions. Details pertaining to the injection of the DLW solution, blood collection, preparation and analysis of plasma samples, and calculation of energy expenditure are provided in Fournier et al. (2002). We analyzed energy expenditure data using analysis of covariance (ANCOVA), adjusted for body mass as a covariate to determine differences between radiomarked and unmarked groups and between wild and captive birds. Body mass and field metabolic rate values were log-transformed. Body mass of radio-marked and unmarked chicks reared in captivity was measured daily and body length was measured every 3 to 5 d. Males and females were pooled for analyses as sex-related differences in growth were found to be minimal until about day 42. Logistic and Gompertz growth curves were fit to the first 38 d of these data and assessed for goodness of fit. We determined that the Gompertz function provided a superior fit to the data based on Akaike s Information Criteria (AIC). We fitted Gompertz growth models that included a random effect for asymptotic size and assumed the repeated measurements were serially correlated with the correlation inversely proportional to the time interval between measurements. Determination of chick mortality and survival rates. Radio-marked loon chicks were located one to several times daily. Transmitters were thermistor-regulated for remote monitoring of loon chick body temperatures and served as a mortality cue. Dead birds were recovered as quickly as possible. Determination of the cause of death was based on recovery location of the carcass and/or transmitter and related evidence. Fresh carcasses were submitted for complete pathological examinations, including selected diagnostic and histopathology studies to check for viruses, bacteria, and parasites. Because the transmitters had a limited life, we recaptured chicks at night and replaced expiring transmitters. The transmitter implant technique was similar to that used with day-old chicks. Transmitter removal and implantation of replacement transmitters was completed in a single surgical procedure. Chicks were returned to within the visual range of parents following surgery and the next day we confirmed that chicks had rejoined their parents. Survival of control and radio-marked chicks was determined by visual observations. The sibling chick served as a control when available (in some cases, the egg that remained in the nest was depredated). Chicks were visually located daily. Survival rates of radio-marked and unmarked loon chicks were calculated using the Kaplan-Meier approach (Kaplan and Meier 1958). A log rank 2 test was used to test for differences between the survival of radiomarked and unmarked chicks. RESULTS We collected and incubated 19 Common Loon eggs in All of the eggs hatched and 12 of these chicks were radio-marked and returned to nests, one chick was returned unmarked, and six chicks were reared in captivity. Average mass of the radiomarked chicks was (SD) g. The duration of the surgical implant procedure averaged 9.4 min (range 7 to 11 minutes) including induction of anesthesia (x 5.6 min) and actual surgery (x 3.8 min). Two of 12 (17%) transmitters im-

5 Vol. 74, No. 2 Radio Transmitters and Common Loons 183 Fig. 1. Percent of time wild unmarked and radio-marked Common Loon chicks were observed resting, swimming, brooding, feeding, and preening, and percent of time chicks were on an adult s back, under an adult s wing, on the water 1 m from an adult, and on the nest at northern Wisconsin study lakes, June planted at hatch were lost, providing a 21-d retention rate of 0.79 using the Kaplan-Meier approach. Eight replacement transmitters (replaced at average age of 21 d; range 10 to 29 d) were all retained through fledging. Chick release. Radio-marked chicks were released to nests within 11 h of hatching (x 6.3 h, range 3 to 11 h). On our approach to a nest, tending adults varied in their reaction from slipping off the nest and quietly remaining within 5 m of the nest to flushing, vocalizing, and moving several hundred meters from the nest. Tending adults returned to nests and assumed incubating/brooding posture within 3 to 77 min (x 22.3 min). In two cases, the radio-marked chick was released to nests where the sibling egg had been depredated but the adults continued to incubate the plastic dummy egg. In three instances, the control chick had hatched. Through observation we confirmed that all of the restrained radio-marked and control chicks escaped the paper towel envelope and were accepted by the adults. Behavior evaluation. We collected 10,484 behavioral observations on 11 radiomarked and eight unmarked loon chicks in the wild totaling 87.4 h. During these observations we observed no impairment of radio-marked chicks and no marked differences in the behavior of radio-marked vs. unmarked chicks. Paired observations (3626 observations totaling 30.2 h) of four sets of chicks lended themselves to further analysis. While time activity budgets varied significantly (MANOVA; Wilks 0.001, F 18.11, P 0.03) among loon broods, radio-marked and unmarked chicks did not differ (MANOVA; Wilks 0.25, F 1.00, P 0.61) in the proportion of time the chicks spent resting, locomoting, brooding, feeding, and preening (Fig. 1). Similarly, while the spatial relationship of chicks to adults varied (MANOVA; Wilks , F , P 0.001) among broods, radio-marked and unmarked chicks did not differ (MANOVA; Wilks 0.25, F 1.00, P 0.61) in positioning with respect to adults (Fig. 1). We collected 10,800 behavioral observations on three radiomarked and three unmarked loon chicks in captivity totaling 45 h (Fig. 2). Observations were analyzed for two time periods, when chicks were 8 d old and when they were 8 d old. Time activity budgets did not vary between radio-marked and unmarked chicks (MANOVA; Wilks 0.16, F 1.71, P 0.50) or with age category (MANOVA; Wilks 0.12, F 2.54, P 0.43). While the proportion of time spent in the water differed with age (ANOVA; F , P 0.02),

6 184 K. P. Kenow et al. J. Field Ornithol. Spring 2003 Fig. 2. Percent of time captive unmarked and radio-marked Common Loon chicks were observed resting, swimming, and preening, and percent of time chicks were on a brooding platform or on the water in a laboratory setting at the Upper Midwest Environmental Sciences Center, June there was no significant effect of radiomarking (ANOVA; F 0.470, P 0.54). Daily energy expenditure and growth. Problems with sample analyses and inability to consistently recapture wild chicks limited our calculations of daily energy expenditure of 10- d old wild and captive chicks and 21-d old wild chicks. Energy expenditures of wild radiomarked birds averaged 6 to 10% higher than those of unmarked birds when comparing paired sample means at ages 10 (6%), 21 (10%), and 35 (7%) d (Fig. 3). Two-way AN- COVA indicated that energy expenditure among sources (wild vs. captive; F 0.278, P 0.626), treatment (radio-marked vs. unmarked; F 0.524, P 0.509), and interaction effects (F 0.387, P 0.567) were not significantly different among chicks 35 d old. We did not detect differences in asymptotic mass ( 2 1 2, P 0.16), instantaneous growth rate ( , P 0.11), or inflection point ( , P 0.08) between radio-marked and unmarked captive chicks. In addition, we did not detect an effect of radio-marking on body length (P 1 for asymptotic mass, instantaneous growth rate, and inflection point). Chick mortality and survival rates. We monitored the daily survival of 12 radio- Fig. 3. Energy expenditure (kj/d) of unmarked and radio-marked Common Loon chicks that were captivereared or monitored in the wild at northern Wisconsin study lakes, June and July 1998.

7 Vol. 74, No. 2 Radio Transmitters and Common Loons 185 marked and nine unmarked chicks. One of the radio-marked chicks was eliminated from the analysis as the timing of the fate of its sibling was not determined. At the end of the field season, eight radio-marked chicks and six unmarked chicks remained alive. Contributing causes of mortality of the radio-marked chicks were attack by an intruding adult loon of a single 1-d-old chick, aquatic predator (e.g., large fish) of a 1-d-old and an 11-d-old chick, and infestation of intestinal parasites of a 38-d-old chick. The 80-d survival rate did not differ (log rank , P 0.92) between radiomarked ( [SE], N 11) and unmarked chicks ( , N 9). DISCUSSION The modified transmitter implant technique we describe shows promise to determine the causes and timing of mortality and the daily survival rate of Common Loon chicks from hatching to fledging. We observed no significant differences in behavior, growth, energy expenditure, and survival between radio-marked and unmarked chicks. However, we note that energy expenditures of wild radio-marked birds averaged 6 to 10% higher than those of unmarked chicks. The small sample size may have precluded detection of a significant effect at 35 d. Only one other published study has assessed the field metabolic costs of radio-marking birds. Klaassen et al. (1992) also reported a higher (7.3%), but non-significant, daily energy expenditure for Common Terns (Sterna hirundo) equipped with transmitters glued to the skin of the interscapular region. Subcutaneous transmitter implants, similar to those used in our study, in Mallard (Anas platyrhynchos) ducklings in an open-circuit respirometer did not significantly affect net heat production (Bakken et al. 1996). If the difference in energy expenditure between wild radio-marked and unmarked loon chicks was real in this study, there was no indication that the birds consequently modified their behavior. The attachment technique offered good transmitter retention: initial transmitters (implanted at hatching) had a 21-d retention rate of All replacement transmitters were retained through fledging. This performance was a marked improvement in retention over the 1.5-g transmitter used in 1997 when all three of the chicks that survived past 15 d lost their transmitters within 6 to 11 days. Comparable size transmitters (1.5 g) have been used with day-old ducklings (about 4% of body mass) without significant retention problems (Korschgen et al. 1996a). One cannot assume that species with closely related body configurations will tolerate a comparable transmitter. A species-specific assessment of transmitter attachment techniques is needed. Subcutaneously implanted transmitters have also proved effective in identifying causes of mortality. Careful monitoring of transmitter temperature, and consequently chick body temperature, can lead to the timely recovery of chick remains and associated evidence following death. In our investigations of loon chicks, we were able to link mortality to disease and predators, the latter including the Bald Eagle (Haliaeetus leucocephalus), fishers (Martes pennanti), and fish. Krementz and Pendleton (1991) found that implanted transmitters provided more accurate information on causes of mortality in ducklings than did externally attached transmitters. We suspect that most telemetry attachment methods have some negative effects. When planning avian telemetry studies, biologists first must consider the impacts of attaching a transmitter to a bird as it relates to the objectives of their study. Evidence to support use of a particular technique should be age and species-specific and address effects on behavior, growth, energetics, and survival. Researchers should weigh published evidence in lieu of conducting their own evaluation. When necessary, evaluations should be incorporated into telemetry studies and include both field and captive work. Because chick survival is strongly related to the chick-adult bond immediately following hatching, we recommend controlled measurement of assembly behavior of chicks released some distance from the adult(s) or systematic flushing of the adult to observe chick following behavior. We also recommend that investigators consult with appropriate veterinary or wildlife professionals to assist with selection of techniques and to obtain the training needed to correctly attach or implant transmitters. The subcutaneous implant technique described here should be used only by experienced individuals after they have received proper training, have dem-

8 186 K. P. Kenow et al. J. Field Ornithol. Spring 2003 onstrated competence in the technique, and have the necessary equipment and supplies in hand. ACKNOWLEDGMENTS This project was funded by the Wisconsin Department of Natural Resources and the Upper Midwest Environmental Sciences Center. We thank R. DeWald, J. E. Lyon, K. A. Kroc, M. L. Meier, L. E. McColl for assistance with field observations and loon chick care; C. E. Korschgen for guidance and logistical support; L. Johnson for providing veterinary consultation; J. Pichner for consultation on captive rearing methods; and F. P. Meyer, L. E. Holland-Bartels, and two anonymous reviewers for providing reviews of the manuscript. LITERATURE CITED AEBISCHER, N. J., P. A. ROBERTSON, AND R. E. KEN- WARD Compositional analysis of habitat use from animal radio-tracking data. Ecology 74: ALTMANN, J Observational study of behavior: sampling methods. Behaviour 49: BAKKEN, G. S., P. S. REYNOLDS, K.P.KENOW, C.E. KORSCHGEN, AND A. F. BOYSEN Thermoregulatory effects of radiotelemetry transmitters on Mallard ducklings. Journal of Wildlife Management 60: BARR, J. F Aspects of Common Loon (Gavia immer) feeding biology on its breeding ground. Hydrobiologia 32: EVERS, D. C A replicable capture method for adult and juvenile Common Loons on their nesting lakes. In: Proceedings from the 1992 conference on the loon and its ecosystem: status, management and environmental concerns (F. Stockwell, ed.), pp North American Loon Fund, Holderness, NH Activity budgets of a marked Common Loon (Gavia immer) nesting population. Hydrobiolgia 279/280: FOURNIER, F., W. H. KARASOV, M.W.MEYER, AND K. P. KENOW The daily energy expenditures of free-ranging common loon (Gavia immer) chicks. Auk 119: HARAMIS, G.M.,AND A. D. NICE An improved web tagging technique for waterfowl. Journal of Wildlife Management 44: KAPLAN, E. L., AND P. MEIER Nonparametric estimation from incomplete observations. Journal of the American Statistical Association 53: KLAASSEN, M., P. H. BECKER, AND M. WAGENER Transmitter loads do not affect the daily energy expenditure of nesting Common Terns. Journal of Field Ornithology 63: KORSCHGEN, C. E., K. P. KENOW, W.L.GREEN, M.D. SAMUEL, AND L. SILEO. 1996a. Technique for implanting radio transmitters subcutaneously in dayold ducklings. Journal of Field Ornithology 67: ,,, D. H. JOHNSON, M.D. SAM- UEL, AND L. SILEO. 1996b. Survival of radio-marked Canvasback ducklings in northwestern Minnesota. Journal of Wildlife Management 60: KREMENTZ, D. G., AND G. W. PENDLETON Movements and survival of American Black Duck and Mallard broods on Chesapeake Bay. Proceedings of the Annual Conference of the Southeastern Association of Fish and Wildlife Agencies 45: LIFSON, N., AND R. M. MCCLINTOCK Theory of use of the turnover rates of body water for measuring energy and material balance. Journal of Theoretical Biology 12: MCINTYRE, J. W The Common Loon: spirit of northern lakes. University Minnesota Press, Minneapolis, MN. MEYER, M. W., D. C. EVERS, T.DAULTON, AND W. E. BRASELTON Common Loons (Gavia immer) nesting on low ph lakes in northern Wisconsin have elevated blood mercury content. Water, Air, and Soil Pollution 80: MINEAU, P., AND M. PEDROSA A portable device for non-destructive determination of avian embryonic viability. Journal of Field Ornithology 57: NAGY, K. A CO 2 production in animals: an analysis of potential errors in the doubly-labeled-water method. American Journal of Physiology 238: R466 R The doubly labeled water method: a guide to its use. Publication , University of California, Los Angeles, CA. PICHNER, J., AND M. W. DONCARLOS Hatching and rearing of the Common Loon (Gavia immer). American Association of Zoological Parks and Aquariums Annual Proceedings: RICKLEFS, R. E Energetics of reproduction in birds. In: Avian energetics (R. A. Paynter, ed.), pp Publications of the Nuttall Ornithological Club 15, Cambridge, MA. TITUS, J.R.,AND L. W. VANDRUFF Response of the Common Loon (Gavia immer) to recreational pressure in the boundary waters canoe area, northeastern Minnesota USA. Wildlife Monographs 79.