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Effects of added lipids on digestibility and nitrogen balance in oiled common murres (Uria aalge) and Western Grebes (Aechmophorus occidentalis) fed four formulations of a critical care diet.

Abstract: Nutritional support is a primary therapy administered to oiled animals during responses to oil spills, but data informing nutritional decision-making during events are limited. In this study, 44 common murres (Uria aalge) and 6 Western grebes (Aechmophorus occidentalis), naturally oiled by oceanic seeps off the coast of Ventura and Santa Barbara Counties, CA, USA, were assigned to 1 of 4 groups fed diets with varying levels (6.8% [no added oil], 11%, and 20%) and types (salmon, corn) of oil added to a partially purified basal diet. Birds used in the study ranged from extremely emaciated to thin body condition (62%-80% wild bird mean body mass). Acid-insoluble ash was used as an indigestible dietary marker to quantify nitrogen retention, apparent nitrogen digestibility, nitrogen-corrected apparent metabolizable energy, energy digestibility, fat retention, fat digestibility, and estimated fat excretion. Fat excretion is important in these species because once birds have been cleaned they are at risk of plumage recontamination from excreted fat during care. Lower fat diets resulted in lower fat excretion but higher nitrogen retention, higher apparent nitrogen digestibility, and higher apparent metabolizable energy. Decreases in nitrogen retention were significantly related to increases in fat excretion. Regardless of diet, energy digestibility significantly declined with declines in body mass, suggesting severity of emaciation reduced a birds' ability to extract energy from food. Energy digestibility was highest in the 11% (low) salmon oil diet; hence, this diet had the highest effective energy content despite a lower gross kcal/kg diet. Diets fed during oil spills historically have had high fat concentrations to provide maximum caloric support. Results of this study suggest that lower fat diets may be more efficacious for nutritionally depleted seabirds. This study provides valuable data to guide clinical decision making regarding nutritional support during oil spills and other mass stranding events.

Key words: Digestibility, fat excretion, nutrition, oil spill, rehabilitation, avian, seabirds, common murres, Uria aalge, Western grebes, Aechmophorus occidentalis


Nutritional support is a primary therapy administered to oiled animals during responses to oil spills. Historically, feeding protocols for aquatic birds during events, such as the Exxon Valdez oil spill in Alaska in 1989 and the Cosco Busan oil spill in San Francisco Bay in 2007, have been based on the natural history of affected species when wild and healthy, extrapolation from nutrient requirements of domestic avian species, and the practical collective experience of veterinary personnel and wildlife rehabilitators. In California, wildlife response during oil spills is managed by the Oiled Wildlife Care Network (OWCN), (1) housed within the Wildlife Health Center, School of Veterinary Medicine, University of California, Davis. Since long before the publication of the first edition of OWCN's Protocols for the Care of Oil-Affected Birds in 2000, it has been recognized that significant knowledge gaps exist regarding the nutritional needs of commonly oiled species.

Collecting objective clinical nutritional information relevant to birds treated during oil spills is complicated by several factors. Oiled animals may be used as evidence in legal proceedings and may not be available for research. Disaster-activated wildlife centers tend to be too chaotic for detailed data collection. Marine avian species tend to be faunivores (eg, carnivores, piscivores, zooplanktonivores, molluscivores, and so forth); literature on nutritional or veterinary research involving any faunivorous avian species is sparse, and these studies primarily examine healthy raptors. (2-4) A few studies have examined metabolic changes associated with fasting. (5-7) Several species at risk of oiling (eg, loons [Gavia species] and grebes) are rarely kept in captivity in zoos or aquaria even when healthy because of rapid development of captivity-related lesions. (8) Acquiring nutritional data also is impeded by a dearth of appropriate laboratory models. Mallards (Anas platyrhynchos) are superficially similar to species of concern but are not obligate faunivores and may be taxonomically quite distant from affected species. Purposecaught, healthy wild conspecifics may differ substantially from actual oiled animals in physiologic condition. A large proportion of birds entering care may be in extreme catabolic states. (9)

The nutritional needs of dogs and cats are known to change when animals are in a debilitated state. (10-11) Consequently, it is reasonable to expect that the nutritional status of birds admitted for care during oil spills may pose a distinct challenge to successful rehabilitation. Additionally, when nonoiled conspecifics enter routine rehabilitative care, the organizations that provide care are primarily humanitarian or environmental organizations dedicated to best practices in treating individual wild animals as veterinary patients. Research that interferes with the rehabilitation progress of individual animals at these facilities generally is unacceptable and must be conducted with standards of care and individual patient concern more closely resembling clinical trials involving human patients or companion animals than those standards applied to experiments designed to determine optimal nutrition. Nonoiled animals admitted to rehabilitation facilities also may possess a diversity of health problems. Consequently, laboratory animals, wild healthy conspecifics, and nonoiled conspecifics undergoing rehabilitation for other reasons may be unsuitable for answering questions regarding the nutritional needs of oiled seabirds.

Each year, the Los Angeles Oiled Bird Care and Education Center (LAOBCEC) facility managed by International Bird Rescue receives 100 to 500 aquatic birds affected by oiling that are not associated with a responsible party but rather have been oiled by natural seeps that occur off the Santa Barbara and Ventura County coasts. International Bird Rescue provides treatment for these animals during ordinary operations rather than as part of a declared emergency response. Although the oil to which these birds are exposed may differ chemically from refined products or from crude oil from other geographic areas, the affected birds present for care with the same clinical problems as birds oiled during anthropogenic events. Clinical signs are hypothermia, emaciation, anemia, hypoproteinemia, and skin lesions from exposure to caustic materials. (12) Species affected by this ongoing oiling event are the same as those affected during actual coastal oil spills in California (eg, alcids, grebes, loons, diving ducks, procellarids, and pelicans).

Historically in California and during large responses elsewhere, such as the Exxon Valdez oil spill in 1989 (Holcomb J, oral communication, April 2014), commercial nutritional products administered to birds included Pedialyte and vanilla Ensure (Abbott Laboratories, Abbott Park, IL, USA). (1) Other diets commonly gavaged were slurries made of blended whole fish with added vanilla Ensure and vitamin supplementation, or slurries made from ground flamingo breeder diet or commercial waterfowl diets (Mazuri; PMI Nutrition International, Richmond, IN, USA). These diets include substantial carbohydrate components, from glucose to sucrose and more complex carbohydrates. Carbohydrates more complex than glucose require specific enzymes for breakdown. Strict faunivorous birds are unlikely to have the range and quantities of carbohydrases needed to digest diets enriched in starches or sucrose. Undigested sugars in feces may cause osmotic diarrhea. (13) Dietary carbohydrates, with the exception of chitin, are nearly absent in diets of marine faunivorous birds and are of limited use in carnivorous birds, such as black vultures (Coragyps atratus), that engage in obligatory gluconeogenesis to maintain blood glucose concentrations. (2,14) Barn owls (Tyto alba) experience extended episodes of hyperglycemia when administered glucose-containing diets, (3) as do American kestrels (Falco sparverius), which also exhibit diarrhea when fed moderate levels of starch or glucose. (15) Diets fed to kestrels containing gelatinized or native starch had lower apparent metabolizable energy than a high-protein base diet without starch. (15) The effective energy content of high carbohydrate foods may be much lower than expected if birds are not actually able to use these carbohydrates as an energy source due to lacking the necessary enzymes or transporters.

As part of the advancement of oiled-bird feeding protocols away from high carbohydrate foods, diets designed specifically for carnivorous animals started being fed routinely to avian aquatic faunivores undergoing rehabilitation in California in approximately 2009. To maximize caloric intake, high fat diets were fed, but it was observed that if these diets were fed to inappetent piscivores kept in water, birds were at high risk of suffering waterproofing problems due to plumage contamination from steatorrhea. Excreted fats were observed to form an oily slick on the surface of pools. This problem stimulated the questions: how much fat should be fed to maximize metabolizable energy absorption while minimizing excretion of dietary lipids, and does it matter what kind of oil is used? Corn oil is a commonly used feed ingredient, and although it contains significant amounts of polyunsaturated fatty acids (PUFAs), these are almost entirely n-6 [C.sub.18] fatty acids, while fish oils, such as salmon oil, have large amounts of longer chain n-3 fatty acids. (16) In broiler chickens, higher ratios of PUFAs to monounsaturated and saturated fatty acids increases digestibility of dietary fat. (17,18) In piscivorous marine fish, such as salmon, digestibility of dietary lipids is correlated negatively with higher levels of saturated fatty acids. (19)

The purpose of this study was to acquire objective digestibility data to inform choices regarding nutritional support during rehabilitation of avian obligate faunivores during oil spills. Specific aims were to: (1) assess nitrogen balance during the testing period, (2) assess nitrogen-corrected apparent metabolizable energy of test diets, (3) assess fat digestibility at different concentrations of salmon oil, (4) compare fat digestibility between two different primary oils (salmon vs corn oils), and (5) calculate the estimated maximum amount of fat excreted by birds fed the different diets as an index of plumage fouling potential.

Materials and Methods

Study design

Common murres (Uria aalge) and Western grebes (Aechmophorus occidentalis) naturally oiled by offshore petroleum seeps at the Ventura and Santa Barbara County coasts in southern California and presented for care at the International Bird Rescue wildlife clinic at LAOBCEC were enrolled in the study. Birds entered the study upon arrival at the rehabilitation center in a presumably unfed state, and most exhibited emaciation, hypothermia, dehydration, and/or dermal burns from exposure to oil. Birds that arrived for care in extremely poor condition where death or euthanasia was highly likely were excluded from enrollment.

Options for evaluating the digestibility of diets in birds were assessed for feasibility in clinical rehabilitation circumstances, including total fecal collection and use of indigestible dietary markers. (20-27) In a preliminary study, it was found that chromium oxide ([Cr.sub.2][O.sub.3]) could be mixed into a powdered diet without difficulty but was not well-dispersed when reconstituted into a liquid diet, where clumping and adherence to container walls was problematic. Thus, acid insoluble ash was selected for use in this study.

Emeraid Piscivore (Lafeber Company, Cornell, IL, USA), a semi-purified diet intended for debilitated piscivorous species, was mixed with acid insoluble ash (AIA; Celite; Sigma-Aldrich Corp., St Louis, MO, USA) at 2% dry matter. This diet is formulated to be supplemented with added oil (up to 35% fat), and the powder mix includes sufficient essential fatty acids from corn oil and canola oil to meet expected requirements for these nutrients without added oil. Ingredients of the powdered base diet includes soy protein hydrolyzate, canola oil, corn oil, corn syrup solids, cellulose, defatted wheat germ, glutamine, ground limestone, dicalcium phosphate, DL-methionine, potassium chloride, magnesium sulfate, L-lysine, cysteine, taurine, tryptophan, vitamin A supplement, vitamin E supplement, vitamin D3 supplement, menadione sodium bisulfite complex, ethoxyquin, copper sulfate, manganese oxide, zinc oxide citric acid, mixed tocopherols, niacin supplement, calcium dipantothenate, riboflavin supplement, thiamine mononitrate, pyridoxine hydrochloride, vitamin B12 supplement, folic acid, biotin, ascorbic acid, and sodium selenite. More detailed composition of the diet is proprietary. Composition of four test diets is described in Table 1 and included 2 levels of total fat, 2 types of added oil (salmon and corn), and no added oil at all. Diets were designated as basal diet (BD), low salmon oil (LSO), high salmon oil (HSO), and high corn oil (HCO).

For this study, 44 murres were enrolled: 9 were fed BD, 11 LSO, 9 HSO, and 14 HCO. Numbers of Western grebes entering care during the enrollment period were lower than expected and only 6 birds were enrolled: 5 were fed HSO and 1 fed BD. Feeding 4 different test diets to birds simultaneously was deemed not feasible because the work environment made it highly likely that individual birds would occasionally be provided the wrong diet. Thus, birds were enrolled in randomized blocks of 5 in order of arrival. Four test pens were available, which ensured that no more than 2 diets were in use at any one time. All diets were fed during at least 2 different time periods to avoid confounding treatment and time. All birds enrolled were after hatch year adults and sex was unknown. The University of California, Davis Institutional Animal Care and Use Committee approved all experimental procedures.

Standard soft-sided (tarp), net-bottom pens used to house highly aquatic species were modified to accommodate trays for collection of droppings. Each pen was approximately 2 X 1 X 1 m, with fabric sheeting used as a top cover. Birds were housed indoors (68[degrees]-72[degrees]F [20[degrees]-22.2[degrees]C]) at LAOB-CEC during the study, with natural day/night cycles. When housed in the net-bottom pens, birds were protected from development of captivity-related leg lesions by applying soft cotton "booties" to protect delicate leg and foot structures, such as interdigital webbing, toenails, and plantar surfaces of toe joints. In addition to soft cotton booties, keel cushions were fitted to grebes to prevent keel lesions. The murres tend to stand in dry housing and did not require keel protection.

After arrival at the facility, birds were initially hydrated orally with warm isotonic saline (50 mL/ kg) once and then started on a feeding schedule of the assigned test diet. Birds were fed solely the test diet while on the study. Between days 1 and 4, when physiologic criteria necessary to be eligible for washing were met (active and alert, packed cell volume [PCV] [greater than or equal to] 30%, and total plasma solids > 2.5 g/dL), birds left the study and rejoined the rehabilitation population. (1) Birds varied in the number of days required to meet these criteria. Droppings were collected once daily at 9:00 AM. Powdered Emeraid Piscivore with the appropriate added oil was reconstituted with warm tap water to a density suitable for the hydration status of each patient (ie, severely dehydrated birds were fed a higher percent water) and fed at 100[degrees]F (37.8[degrees]C) and 50 to 70 mL/kg body mass 7 times daily (every 90 minutes) by gavage tube. Diet was made fresh daily. Birds were weighed daily before the first meal of the day. Final disposition (died, euthanized, or released) of each animal was recorded.

Droppings were stored in plastic specimen bags and frozen at -20[degrees]F (-28.9[degrees]C) until analysis. Droppings collection resulted in 1 to 4 discrete samples per bird. Samples were freeze dried, homogenized with mortar and pestle, and analyzed at Eurofins Scientific (Petaluma, CA, USA), for nitrogen, crude fat, ash, acid insoluble ash, and energy. Three samples of each diet were analyzed for nitrogen, crude fat, ash, acid insoluble ash, and energy, and average values for each test diet were used in subsequent calculations. Crude fat was measured by the acid hydrolysis method, nitrogen was measured by combustion, ash was determined by ashing in a muffle furnace, and acid insoluble ash was determined by ashing in a porcelain crucible followed by acid digestion, filtration onto ashless filter paper, and ashing again. (28-31) Energy was determined by bomb calorimetry by exploding a 1-g sample and measuring the increase in heat produced (Parr Instrument Co, Molene, IL, USA). Diet samples representing a range of densities as fed were assessed for percent dry matter by weighing before and after freeze drying in the Nutrition Laboratory at the Animal Science Department, University of California, Davis to confirm the range of percent solids fed.


Nitrogen retained (NR), apparent nitrogen digestibility (ApND), apparent metabolizable energy corrected for nitrogen excretion (AMEn), energy digestibility (ED), fat retained (FR), and fat digestibility (FD) were calculated by using the following equations (dry matter basis):

NR (%) = [] - [([N.sub.excreta] X [])/[AIA.sub.excreta]]

ApND (%) = (NR/[]) x 100

AMEn (kcal/kg diet) = [] - [(C[E.sub.excreta] X [])/[AIA.sub.excreta]] - 8.22 X [N.sub.retained]

ED (%) = AMEnl[] X 100

FR (%) = [] - [([Fat.sub.excrta] X [])/[AIA.sub.excreta]]

FD (%) = ([Fat.sub.retained]/ []) x 100

where NR is the percent of nitrogen from diet retained by the bird; [N.sub.diel] and [N.sub.excreta] are the percents nitrogen of the diet and droppings, respectively; [] is the percent AIA in the diet; [AIA.sub.excreta] is the percent AIA in droppings; ApND is the percent of nitrogen ingested by the bird that was absorbed; AMEn is nitrogen-corrected apparent metabolizable energy content of the diet in kcal/kg; [] is the gross energy of the diet in kcal/kg dry matter; [GE.sub.excreta] is gross energy of droppings in kcal/kg dry matter; 8.22 is the energy value of uric acid in kcal/g; ED is percent energy from diet that was used by the bird; FR is the percent fat retained by the bird; [Fat.sub.diel] is the percent fat present in the diet; and FD is the percent of ingested fat that was absorbed by the bird. (32-34)

Estimated fat excretion (FE) calculations:

Body mass X 70 mL/kg X 7 meals/day = mL diet/ day

mL diet/day X % dry matter (high estimate) = g dry matter fed/day

g dry matter fed/day X % fat of diet = g fat fed/day

1 - % fat retained = % fat excreted

% fat excreted X g fat fed/day = g fat excreted/day

g fat excreted/day/0.9 g/mL density of oil = mL oil excreted/day

Data analysis

Seven outcome variables (NR, AMEn, ApND, ED, FR, FD, FE) were calculated for each sample and assessed for normality by Shapiro-Wilk tests. Descriptive statistics, including mean, standard deviation (SD), median, and range for body mass of birds enrolled in each treatment group, and all outcome variables were computed by using Microsoft Excel (Microsoft Corporation, Redmond, WA, USA). Diet groups were compared by using Kruskal-Wallis or 1 -way ANOVA tests. Statistical tests were performed using JMP statistical software (version 10, SAS Institute, Cary, NC, USA). Results were considered significant if P < .05; P values between .05 and .10 were considered trends. Results are reported as mean [+ or -] SD.


Diets were fed at densities ranging from 15% to 20% solids. Both high fat diets were intended to be fed at 20% fat but analysis showed a small difference between HSO and HCO (21% vs 19% fat, respectively). Body mass of murres in each treatment group at admission is presented in Table 2. Murres enrolled in BD and LSO diets were approximately 50 g heavier on average than birds fed diets HCO or HSO, but this difference was not significant (P = .23). These body masses suggest extremely poor nutritional condition in all treatment groups, with the average animal at or below body mass where fat stores have been depleted (ie, < 675 g for adult murres (8)) compared to a body mass range of 805 to 1175 g in wild birds. (35)

AMEn, ApND, and maximum (at 20% solids) estimated FE by diet fed are displayed in Figure 1. None of the 7 outcome variables was normally distributed, nor were transformations thereof; however, AMEn and ApND were normally distributed when data from the HCO diet were excluded. None of the 7 outcome variables changed significantly by day of collection whether considered simultaneously or by diet treatment (P range, .34-.94).

As shown in Figure 1, values from day 1 samples did not differ significantly by diet for AMEn (P = .22) or ApND (P = .12) but did differ significantly for FE (P = .008). When data from all days were considered, all 3 variables were significantly different (AMEn, P = .002; ApND, P= .001; FE, P < .001) by Kruskal-Wallis tests. When HCO data were excluded and 1-way ANOVA was used to examine the relationships of diet identity to AMEn, ApND, and ED on day 1, values tended to be higher for LSO than BD or HSO for AMEn, ApND, and ED but results were not significant (P = .07, .09, and .12, respectively). Values for LSO were significantly higher than other diets when data from all days were compared (P < .001, P < .001, and P = .003, respectively). The LSO was the only diet where the SD of ApND did not extend below zero, where negative values indicate a negative nitrogen balance. The highest value for ED was with LSO on day 1 (68% [+ or -] 17% compared to 50% [+ or -] 20% for HSO, 52% [+ or -] 24% for BD, and 52% [+ or -] 23% for HCO) and across all days (69% [+ or -] 13%, compared to 52% [+ or -] 19% for HSO, 51% [+ or -] 22% for BD, 59% [+ or -] 22% for HCO).

The FR% significantly increased with increased fat in the diet whether considered for day 1 alone or all days (both P < .001). The BD (lowest percent fat) showed the lowest fat retention values while HSO (highest percent fat) showed the highest fat retention values. Both LSO and HCO had intermediate values. The digestibility of dietary fat (percent of ingested fat retained by the bird) was not significantly affected by diet either on day 1 (P = .68) or on all days (P = .40). Day 1 fat digestibility was 67% [+ or -] 23% for BD, 75% [+ or -] 22% for LSO, 64% [+ or -] 28% for HSO, and 66% [+ or -] 22% for HCO. Fat digestibility for all days was 73% [+ or -] 20% for BD, 77% [+ or -] 17% for LSO, 65% [+ or -] 24% for HSO, and 70% [+ or -] 20% for HCO. The FE values were significantly lower for the 2 lower fat diets than for the 2 higher fat diets when considered as day 1 alone (P = .008) or all days (P < .001). The HCO and HSO diets did not differ significantly in any of the 7 outcome variables by Student's /-tests (P range, P = A4-P = .92).

Although the proportion of birds surviving to release from each treatment group (BD, 5 of 9 [56%]; LSO, 4 of 11 [36%]; HSO, 2 of 9 [22%]; HCO, 5 of 14 [36%]) appeared to have a negative relationship to increasing percent fat in the diet, this was not found to be significant by least squares regression of percent released against percent fat in diet (P = .13). No significant differences were found among the diet treatments for changes in body mass between days 1 and 3 of the study period (P = .59, n = 33; mean change in mass = 3.8 [+ or -] 36.7 g, median = 4 g, range = loss of 72 g to a gain of 108 g).

In day 1 samples, ApND had a positive relationship to AMEn ([R.sup.2] = 0.649, P < .001, y = 0.00275 x - 0.638) and FD ([R.sup.2] = 0.240, P = .001, y = 0.797 x - 0.374) and a negative relationship to FE ([R.sup.2] = 0.212, P = .003, y = -0.060a + 0.367). No significant relationship was found between ApND and FR (P = .33). Also in day 1 samples, AMEn showed a positive relationship to FR ([R.sup.2] = 0.284, P < .001, y = 116.90ax 1707.3) and FD ([R.sup.2] = 0.627, P < .001, y = 3888.5a + 257.873) and a negative relationship to FE ([R.sup.2] = 0.433, P < .001. y = -256.675a + 3761). When all days were included, ApND showed a positive relationship to AMEn ([R.sup.2] = 0.673, P < .001, y = 0.00269a - 0.615), FR ([R.sup.2] = 0.074, P = .008, y = 0.019a + 0.013), and FD ([R.sup.2] = 0.268, P < .001, y = 0.876a - 0.411) and a negative relationship to FE ([R.sup.2] = 0.231, P < .001, y = -0.055x + 0.379). Also for all days, AMEn had a positive relationship to FR ([R.sup.2] = 0.369, P < .001, y = 129.70a- 1692), FD ([R.sup.2] = 0.573, P < .001, >> = 3963a+ 242), and a negative relationship to FE ([R.sup.2] = 0.336, P < .001, y = -203.6a + 3683).

For the 3-day collection period, the mean [+ or -] SD values for grebes were: BD (n = 3): ApND = 12% [+ or -] 25%, AMEn = 1836 [+ or -]513 kcal/kg diet, FD = 38% [+ or -] 17%, FR = 2.6% [+ or -] 1.2%, FE = 4.9 [+ or -] 1.37 mL/day, and HSO (n = 8): ApND = -29% [+ or -] 42%, AMEn = 2164 [+ or -] 1219 kcal/kg diet, FD = 71% [+ or -] 17%, FR = 5.6% [+ or -] 13.7%, FE = 11.91 [+ or -] 10.16 mL/day. Despite the low numbers of birds enrolled, values followed a similar pattern to those of murres, where birds fed the higher fat diet had lower ApND. Comparison of values for murres and grebes fed HSO showed mean ApND was significantly lower in grebes than in murres (P = .01) by Student's t-test. Other comparisons of values between grebes and murres fed HSO were not significantly different. The FE by grebes was similar to values for murres fed BD and HSO.


As judged from admission body mass, more than half of the birds enrolled in this study were at or below the body mass at which fat stores are near zero and body protein has been markedly catabolized. (9,35) Oiled common murres in extreme catabolic states display intestinal atrophy with fasting, but thickness of the intestinal walls and length of intestinal villi increases with refeeding for 24 to 72 hours. (36) In other avian species undergoing migratory fasting, the intestine and related digestive organs may atrophy to a greater degree than the body as a whole. Recovery to normalized digestive function and food intake after a significant episode of fasting may require several days. (37,38) In birds in a catabolic state entering rehabilitation, gastrointestinal atrophy may affect digestive capabilities during early days of care, especially if protein catabolism has been extensive. Birds in this study showed very minimal changes in body mass over the course of the first 3 days of care; none of the diet treatments resulted in significant weight gains. This finding is in accord with observations of caregivers, which suggest that birds do not generally gain discernible weight until later in care when eating solid food. This study did not show either an increase in AMEn with the passage of days or values of AMEn as high as expected for faunivorous animals. These findings suggest that recovery to normalized gastrointestinal function in these animals may take longer than 1 to 4 days. Causes of this longer recovery are unknown but may simply reflect the severely debilitated state of the birds at the start of the study.

Higher fat diets were shown to result in higher fat retention, that is, birds fed more fat assimilated more fat, but these birds also excreted more fat. This is expected because the digestibility of fat did not differ significantly with differing levels of dietary fat and is clinically relevant in that we did not identify an upper ceiling to the amount of fat these birds are able to digest. While plumage contamination is not an issue for oiled birds awaiting washing, birds often are inappetent after the stress of washing and require supplemental feeding during the transition from dry housing to pools. The process of each bird becoming fully waterproof may take several days. Fat digestibility across all levels of dietary fat in this study was lower than predicted from studies on mallards and chickens, where fat digestibility is greater than 80% in chickens and in excess of 97% in ducks. (18,39,40) Seabird studies show dietary lipid assimilation efficiency >80% for neutral lipids in white-chinned petrels (Procellaria aequinoctialis) and black-footed albatross (Phoebastria nigripes), while rockhopper penguins (Eudyptes chrysocome) showed values of 62% and 45% for 2 radiolabeled neutral lipids. (41) Triglyceride and wax ester assimilation was >90% in Leach's storm petrel (Oceanodroma leucorhoa) chicks. (42) Substantial variation in assimilation of radioactively labeled wax esters due to age was found in least auklets (Aethia pusilla), with values as high as 99% in chicks but as little as 40% in adults. (43) In this study, the type of oil (corn or salmon oil) did not significantly affect the variables measured, although differences may emerge with larger sample sizes or may exist in other polyunsaturated fatty acids.

The low percentage of fat digestibility in our study is likely a result of the catabolic states and presumed intestinal atrophy of the birds. Fat digestion requires sufficient bile precursors, such as taurine and cholesterol, adequate production and secretion of bile to emulsify ingested fat, adequate production of lipases and intestinal capacity for absorption, together with sufficient metabolic energy to perform these and other digestive functions. (44) Bile, which normally is recycled through enterohepatic recirculation, may be lost to feces if intestinal function is impaired by atrophy, epithelial damage due to petroleum exposure, or maldigestion. Failure of bile resorption may lead to fat malabsorption and diarrhea. (45) In this study, fat excretion and apparent nitrogen digestibility were negatively related. In the absence of adequate bile salts and bile phospholipids, proteins and peptides partially emulsify lipid globules. These partially emulsified lipid droplets would likely be poorly absorbed and when excreted may facilitate the loss of emulsifying proteins and peptides. Regardless of the exact mechanism, addition of emulsifying ingredients, such as lecithin, may improve the digestibility of the dietary lipids.

Of the diets examined, results suggest that LSO possesses the most positive characteristics as a critical care diet for gavaging to common murres. Despite having a lower gross energy content than the higher fat diets, LSO displayed higher nitrogen-corrected metabolizable energy, higher nitrogen retention, and lower fat excretion than the higher fat diets in oiled murres. Birds fed higher fat diets excreted more fat and were more likely to show a negative nitrogen balance. This combination would make the high fat diets more likely to cause plumage contamination and less likely to reverse the catabolic state of the birds. Negative nitrogen balance in these birds can only be caused by catabolism of amino acids and consequent excretion of nitrogen in excess of that gained by amino acid absorption from the diet. Basal metabolic rate (BMR) has been estimated to be 593 kJ/day (141.9 kcal/day) for a 1025 g common murre. (46) At 20% solids and 7 meals of 70 mL/kg, the test diets used in this study would provide the hypothetical 1025 g bird with 100.5 g dry matter. Incorporating ED of each test diet into calculations, net energy assimilated would be approximately 244 kcal/day for BD, 352 kcal/day for LSO, 288 kcal/day for HCO. and 278 kcal/day for HSO. Energy requirements of oiled birds in a hospital environment are largely unknown, but illness factors of 0.7 (emaciation) to 2.0 (burns) would apply to typical clinical conditions. (47) In a hypothetical case of a common murre in good body condition (1025 g) with chemical burns, maintenance energy requirement is assumed to be 1.5 X BMR, and if the illness factor for burns of 2.0 is incorporated into calculations, the caloric requirements would be up to 426 kcal/day. The bird in this hypothetical case would not be receiving sufficient energy from the diet, even if fed LSO.

Although Western grebes were not well represented in this study, data showed grebes fed HSO had significantly lower ApND than common murres. Species may have large variation in response to diets, due to differences in normal gastrointestinal physiology, nutritional condition at arrival, or differences in susceptibility to stress in captivity. As two species that may be presented in large numbers for rehabilitative care in California, further investigation into optimal nutritional support for Western grebes and common murres is needed.

When oil spills occur, there often is much debate about the merits of rehabilitating affected animals. However, little research has been done to examine how rehabilitative techniques, such as nutritional support, may affect outcomes. Most oiled birds arriving at rehabilitation facilities in California are not healthy birds that simply need cleaning. (9) Rapid increases in energetic expenditures and other effects of oiling may quickly result in large numbers of extremely debilitated birds presented for care at or near survivable limits of nutritional depletion. Considering the results of this study, past efforts to increase oiled birds' caloric intake through feeding high fat diets may have been counterproductive due to reductions in nitrogen retention, in addition to physical problems associated with excretion of excess fats. Poor nitrogen retention may delay replacement of catabolized tissue components and affect the animal's ability to survive rehabilitative efforts. During future events, birds may be benefited by feeding diets with low or moderate levels of fat. To our knowledge, this study is the first digestibility study completed on actual oiled birds and provides valuable data to guide clinical decision-making regarding nutritional support during future mass stranding events such as oil spills.

Acknowledgments: This project was supported by the California Department of Fish and Wildlife's Oil Spill Response Trust Fund through the Oiled Wildlife Care Network at the Wildlife Health Center, School of Veterinary Medicine, University of California, Davis. We thank the staff and volunteers of International Bird Rescue who cared for these animals and assisted with feeding and sample collection, especially Julie Skoglund and Kelly Berry for their invaluable help with enrollment of birds into the study. We thank Arielle Hines and Guthrum Purdin for assistance with sample processing, and Ted Lafeber for his generosity in providing specially mixed diets for this study.

Rebecca S. Duerr, DVM, MPVM, PhD, and Kirk C. Klasing, PhD

From International Bird Rescue, 4369 Cordelia Rd, Fairfield, CA 94534, USA (Duerr), and Animal Science Department, University of California. Davis, 1 Shields Ave., Davis, CA 95616, USA (Klasing).


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Caption: Figure 1. AMEn, estimated FE, and ApND % (mean [+ or -] SD) in oiled common murres fed 1 of 4 diets. See Table 1 for composition of each diet. P values reflect significance based on Kruskal-Wallis tests; test diets sharing a letter in common do not differ by pairwise Wilcoxon tests.
Table 1. Composition of 4 test diets fed to oiled
common murres and Western grebes.

          Nitrogen.   Protein,           Fat
Diet          %        % (e)     (from basal diet), %

BD (a)      10.1        63.3             6.8
LSO (b)     10.0        62.6             6.4
HSO (c)      9.2        57.5             5.8
HCO (d)      8.9        55.4             5.8

          Added oil.   Total fat,         Acid
Diet          %            %        insoluble ash, %

BD (a)        0           6.8             2.0
LSO (b)      4.7          11.1            1.8
HSO (c)      15.0         20.8            1.9
HCO (d)      13.6         19.4            1.8

          Other ash.   Gross energy,
Diet          %           kcal/kg

BD (a)       6.8           4740
LSO (b)      6.1           5080
HSO (c)      5.7           5340
HCO (d)      6.2           5510

(a) Basal diet with no added oil.

(b) Basal diet plus low amount of added salmon oil.

(c) Basal diet with high amount of added salmon oil.

(d) Basal diet with high amount of added corn oil.

(e) Percent protein shown = %N X 6.25. the multiplication
factor for the typical amount of nitrogen in plant protein.

Table 2. Body mass of oiled common murres (n) in each of
4 treatment groups fed diets with varying types
and amount of fats.

                        Initial body mass, g

Diet       n    Mean (SD) (e)   Median   Range (e)

BD (a)     9      686 (71)       680      592-810
LSO (b)    11     677 (69)       688      574-826
HSO (c)    9      636 (61)       630      534-746
HCO (d)    14     635 (83)       600      510-778

(a) Basal diet with no added oil.

(b) Basal diet plus low amount of added salmon oil.

(c) Basal diet with high amount of added salmon oil.

(d) Basal diet with high amount of added corn oil.

(e) Wild body mass mean = 1022 g, range = 805-1175 g. (35)
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Title Annotation:Original Study
Author:Duerr, Rebecca S.; Klasing, Kirk C.
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Geographic Code:1U9CA
Date:Jun 1, 2017
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