Mississippiensis: Growth e Ects of Lysine in Compounded Diets For American Alligator, Alligator

2023-08-14 14:15 Growth effects of lysine in compounded diets for American alligator, Alligator mississippiensis - Reigh - 2022 - Journal
- Journal of the World Aqua…
Journal of the World Aquaculture Society / Volume 53, Issue 5 / p. 995-1005
APPLIED STUDIES Open Access    
Growth effects of lysine in compounded diets for American alligator, Alligator

mississippiensis
Robert C. Reigh , Millie B. Williams
First published: 05 April 2022

https://doi.org/10.1111/jwas.12884
Citations: 1
Funding information: Cargill Inc.; Louisiana Agricultural Experiment Station; Louisiana Department of
Wildlife and Fisheries, Grant/Award Number: Agreement 2000186281; National Institute of Food and
Agriculture, U.S. Department of Agriculture, Grant/Award Number: Hatch project LAB94282
Abstract
Nutritional requirements of the American alligator, Alligator mississippiensis, are largely
unknown despite the value of farm-raised alligator as an aquaculture product. We
conducted a 10-month growth trial to determine effects of graded levels of dietary lysine
on alligator growth as measured by increase in body length, body weight gain, and free
lysine concentration in blood plasma. One-hundred-ninety-two hatchling alligators were
fed 50% crude protein, pelletized diets, composed primarily of practical feed ingredients,
with 1.5, 2.25, 3.0, or 3.75% dietary lysine. Diets were fed for 326 days under
temperature-controlled, laboratory conditions. Body lengths and body weights were
measured at 60-day intervals, and blood samples were taken at the final weighing.
Increases in body length, body weight gain, and free lysine level in blood plasma
indicated that a concentration of at least 2.25% dietary lysine (as fed)—about 4.5% of
protein—was adequate for growth of alligator under the conditions of this study. Results
suggest that the lysine requirement of American alligator is similar to requirements
reported for other aquaculture species, including some fishes, crustaceans, and
amphibians.
1 INTRODUCTION
Farming of American alligator is the second-largest aquaculture industry in Louisiana,
producing hundreds of thousands of alligators annually (LSU AgCenter, 2020). Although
alligator farming has been practiced in Louisiana for more than 30 years, and the industry is
now among the top five most-valuable animal-production enterprises in the state, little
information is available on the nutritional requirements of captive-reared alligator.
https://onlinelibrary.wiley.com/doi/full/10.1111/jwas.12884 1/17
2023-08-14 14:15 Growth effects of lysine in compounded diets for American alligator, Alligator mississippiensis - Reigh - 2022 - Journal of the World Aqua…
As the industry developed, producers transitioned from the early practice of feeding
alligators waste meat, such as carcasses of nutria, muskrat, and poultry, to feeding
commercially manufactured, compounded diets similar to the extruded feeds used today in
many other types of animal aquaculture (Nickum, Masser, Reigh, & Nickum, 2018). Extruded
feeds currently available to the alligator industry are effective, but lack of information on
optimum concentrations of nutrients for alligator diets can result in production of
overfortified feeds containing excessive amounts of nutrients to avoid dietary deficiencies.
While such diets do produce good growth, they may do so at increased feed cost and
reduced efficiency of nutrient utilization, resulting in higher than necessary feed
expenditures and greater waste loads in production systems.
Among the critical nutrients required in animal diets is lysine, a dietary essential amino acid
(NRC, 2011). Lysine is often one of the first growth-limiting amino acids in animal diets due
to its typically high dietary requirement relative to the amounts of lysine present in most
feedstuffs (NRC, 2011). Information on the lysine requirements of some cultured aquatic
animals has been published (Table 1), but little research-based nutritional information is
available for reptiles. Current recommendations for carnivorous reptiles are best estimates
based on nutrient concentrations of live prey (Nijboer, 2020). We conducted a feeding trial to
evaluate the effects of different concentrations of lysine on growth of captive-reared
American alligator fed formulated diets in a laboratory environment.
a
TABLE 1. Reported dietary lysine requirements of fishes, crustaceans, and amphibians
Species Lysine requirement (% Source

a
of diet)
Atlantic salmon (Salmo salar) 2.0% in 50% CP diet Anderson, Lall, Anderson and McNiven (1993)
2.2% in 44% CP diet Espe, Lemme, Petri and El-Mowafi (2007)
2.4% of diet NRC (2011)
Bullfrog (Lithobates 2.71% in 30.4% CP diet Mansano et al. (2017)

catesbeianus)
Channel catfish (Ictalurus 1.2–1.5% in 24–30% CP diet Wilson, Harding and Garling Jr. (1977); Robinson,
punctatus) Wilson and Poe (1980)
Cobia (Rachycentron canadum) 2.38% of diet Zhou, Wu, Chi and Yang (2007)
Common carp (Cyprinus carpio) 2.2% in 48% CP diet Nose (1979)
European sea bass 2.2% in 50% CP diet Tibaldi and Lanari (1991)
(Dicentrarchus labrax)
Species Lysine requirement (% Source

a
of diet)
Japanese sea bass (Lateolabrax 2.5% in 43% CP diet Mai et al. (2006)
japonicus)
a Adapted in part from Nunes, Sá, Browdy and Vazquez-Anon (2014).
2 MATERIALS AND METHODS

2.1 Animal care and handling
Procedures for animal care and handling were approved by the Institutional Animal Care
and Use Committee of Louisiana State University (protocol number A2019-26).
2.2 Experimental design and dietary treatments

The trial was conducted with 192 hatchling alligators obtained from the Louisiana
Department of Wildlife and Fisheries Rockefeller Wildlife Refuge in Grand Chenier, LA. We
tagged each alligator with a passive-integrated-transponder (PIT) chip (Biomark Inc., Boise,
ID), inserted subcutaneously behind the head. PIT-tagging allowed identification of each
alligator in the event that a problem involving an individual animal arose during the course
of the trial or if we desired to identify individuals at the end of the trial.
Alligators were distributed among 24 tanks (2.44 m long × 1.22 m wide × 0.91 m high), with 8
animals per tank (see Nickum et al., 2018; Figures 1 and 2). Tanks were partially filled with
15 cm of water held at 31°C, the preferred body temperature of alligator (Asa et al., 1998),
via room and tank heaters. Tanks were completely drained, rinsed with warm water, and
filled with 31°C water twice per week.
FIGURE 1
Open in figure viewer PowerPoint

Body weight ± SD of American alligator (initial weight 53.3 ± 5.1 g) fed a graded series of lysine test diets for 326 days.
Diets were formulated with corn gluten, menhaden fish meal, poultry byproduct meal, porcine blood meal, menhaden
fish oil, and a commercial vitamin and mineral premix used in manufactured alligator feeds. Diets provided 1.5, 2.25,
3.0, or 3.75% lysine as percentages of diet weight, as fed
FIGURE 2

Increase in body length of American alligator (mean initial length 26.2 ± 1.1 cm) fed a graded series of lysine test diets
for 326 days. Diets were formulated with corn gluten, menhaden fish meal, poultry byproduct meal, porcine blood meal,
menhaden fish oil, and a commercial vitamin and mineral premix used in manufactured alligator feeds. Diets provided
1.5, 2.25, 3.0, or 3.75% lysine as percentages of diet weight, as fed. Lines within the box plots indicate median (solid) and
mean (dashed) values. Median values of plots that share the same letter are not significantly different (p > .05)
A basal diet, composed primarily of corn gluten meal, menhaden fish meal, poultry by-
product meal, porcine blood meal, and menhaden fish oil, was formulated with MixitWin
software (Agricultural Software Consultants Inc., San Diego, CA) to contain 50% crude
protein, as fed (Table 2). Lysine concentration of the basal diet was set at 1.5% of diet weight
based on concentrations of lysine used in studies with other warm-water aquaculture
species (Table 1). Supplemental arginine was added to the basal diet formulation to
approximate the 1.6-to-1 ratio of arginine-to-lysine in alligator whole body (Reigh &
Williams, 2018) and avoid negative effects of arginine–lysine imbalance on lysine utilization
(Ball, Urschel, & Pencharz, 2007). Taurine supplementation also was provided because corn
gluten meal, a plant product which contains low levels of taurine, composed 55–59% of the
basal diet. Taurine, which is abundant in animal tissues, particularly muscle, serves many
functions in animal bodies (Ripps & Shen, 2012). It is a dietary essential nutrient for cats and
is considered a conditionally indispensable amino acid (at concentrations of 0.1–2%) in diets
of farmed fish and shrimp (El-Sayed, 2014; Gunathilaka et al., 2019; Salze & Davis, 2015).
Additional ingredients included a proprietary vitamin/mineral premix used in commercially
manufactured alligator feeds (Cargill Animal Nutrition, Franklinton, LA),
carboxymethylcellulose as a pellet binder, and powdered cellulose as bulk filler in the diet
formulation. A graded series of four test diets, containing 1.5, 2.25, 3.0, or 3.75% lysine, was
created by adding crystalline lysine to the basal (diet 1) mixture (Table 3).
TABLE 2. Ingredient composition (% as fed) of lysine test diets used in 10-month feeding trial
with American alligator
Ingredient Diet 1 Diet 2 Diet 3 Diet 4
a
Corn gluten 59.41 58.18 56.95 55.66
a
Fish meal, menhaden 10.00 10.00 10.00 10.00
a
Poultry byproduct meal 10.00 10.00 10.00 10.00
a
Blood meal, porcine 1.83 1.83 1.83 1.83
b
Oil, menhaden 10.00 10.00 10.00 10.00
c
L-Arginine, crystalline 1.00 1.00 1.00 1.00
a
Vitamin/mineral premix 1.00 1.00 1.00 1.00
d
Taurine, crystalline 0.50 0.50 0.50 0.50
b
Carboxymethylcellulose 2.00 2.00 2.00 2.00
b
Cellulose, powdered 4.26 4.73 5.19 5.72
e
L-lysine, crystalline 0 0.76 1.53 2.29
a
Cargill Animal Nutrition, Franklinton, Louisiana.
b
Sigma-Aldrich, St. Louis, Missouri.
c
L-Arginine, reagent grade, ≥ 98%, Sigma-Aldrich, St. Louis, Missouri.
d
Taurine, synthetic, ≥ 99%, Sigma-Aldrich, St. Louis, Missouri.
e
L-Lysine monohydrochloride, reagent grade, ≥ 98%, Sigma-Aldrich, St. Louis, Missouri.
a
TABLE 3. Proximate composition (% as fed, calculated) of lysine test diets used in 10-
month feeding trial with American alligator
Protein 50.00 50.01 50.03 50.01
Lysine (% of diet) 1.50 2.25 3.00 3.75
Lysine (% of protein) 3.00 4.50 6.00 7.50
Lipid 12.45 12.42 12.40 12.38
Fiber 7.34 7.78 8.23 8.73
a
Dry matter (%) as fed: diet 1, 93.3; diet 2, 93.4; diet 3, 93.5; diet 4, 93.6.
Prior to pelletizing, dry ingredients were weighed, combined in a twin-shell laboratory mixer
(Patterson-Kelley Co., East Stroudsburg, PA), and mixed for a minimum of 30 min. Mixed
ingredients were moved to a 3-kg capacity, commercial food mixer (Hobart Corp., Troy, OH),
where menhaden fish oil (100 g/kg) was added, and water (approximately 400 ml/kg) was
slowly poured into the mixture until a dough-like consistency was achieved. Diets were
pelletized using a 0.5 HP meat grinder (General Inc., Weston, FL) and air-dried under a fan
for 24 hr. Dry diets were bagged and stored at 4°C until used.
Daily feed allotment per tank was 3% of alligator biomass fed between 09:00 and 11:00 hr.
Prior to data collection, a two-week conditioning period was provided to allow the animals to
become accustomed to the feeds, during which time, consumption of the diets was visually
confirmed in all tanks. Unlike commercially produced extruded feeds, the compression-
pelletized diets used in this trial did not float, but hatchling alligators readily adapted to
eating the sinking feed pellets from the tank bottom.
The primary response variables of interest were increases in body length and body weight
among treatment groups. Initial length and weight (26.2 ± 1.1 cm and 53.3 ± 5.1 g,
respectively) were measured at the end of the conditioning period, and alligators were
weighed and measured at 60-day intervals for 10 months thereafter. Feed allotments were
adjusted after each weighing, and between bimonthly weight measurements, allotments
were increased as necessary to provide as much as the animals would eat with little visible
waste. As the trial progressed, 20 animals that did not eat (i.e., lost weight), died, or were
killed by other alligators were identified by PIT-tag number and removed from the data set.
At the final weighing, blood samples were taken from the ventral coccygeal vein (VCV) of 3
alligators in each tank to compare concentrations of circulating free lysine among treatment
groups. Blood (8 ml) was drawn from the VCV in the tail at a point between the fifth and sixth
scutes behind the right rear leg (see Nevarez, 2007; fig. 10).
Samples were centrifuged for 15 min at 3000 rpm (Forma 1L GP model, Thermo Fisher
Scientific, Waltham, MA). Plasma was removed by pipet and stored at −90°C until analyzed.
Immediately prior to analysis, each sample was filtered through a 0.2 mm PTFE syringe filter
and mixed with 50 μl of internal standard per 100 μl of blood plasma; 0.5 μl of the mixture
was then injected into a high-performance liquid chromatograph (1100 Series, Agilent
Technologies Inc., Santa Clara, CA) equipped with an Eclipse AAA, 4.6 × 150 mm, 3.5 μm
column (Agilent Technologies Inc., Santa Clara, CA) for amino acid separation.
2.3 Statistical procedures

Statistical analyses were conducted with SigmaStat software (Systat Software Inc., San Jose,
CA). One way analysis of variance (ANOVA) was performed to determine if significant
differences (p ≤ .05) in length gain or weight gain occurred among alligators fed the
experimental diets for 326 days. If tests of normality (Shapiro–Wilk) or equal variance
(Brown–Forsythe) failed, Kruskal–Wallis one-way ANOVA on Ranks was performed, followed
by Dunn's method of all pairwise multiple comparisons to identify differences in median
values among groups.
3 RESULTS
Growth of alligators during the 10-month trial was steady but varied considerably among
individuals within treatment groups (Figure 1). Increases in alligator body length were not
normally distributed (p < .05) after 326 days of treatment. One-way ANOVA on Ranks
identified significant differences (p < .001) in median length increases among treatment
groups. Dunn's all pairwise multiple comparisons procedure indicated that length gain of
alligators fed 1.5% dietary lysine was significantly less than length gain of alligators fed
2.25% lysine (p = .001) or 3.75% lysine (p < .001), but not different from length gain of
alligators fed 3% lysine (p = .108) (Figure 2). Length gain of alligators fed 2.25% lysine also
was not significantly different from that of alligators fed 3% lysine (p = .611) or 3.75% lysine
(p = .850); however, length gain of alligators fed 3% lysine was significantly less than length
gain of alligators fed 3.75% lysine (p = .016) (Figure 2).
Weight gain data were normally distributed (p = .762) but not of equal variance (p < .05).
One-way ANOVA on Ranks identified significant differences (p < .001) in median weight gains
among treatment groups. All pairwise multiple comparisons indicated that weight gain of
alligators fed 1.5% dietary lysine was significantly less than weight gain of alligators fed
2.25% lysine (p = .002) or 3.75% lysine (p < .001) but not different (marginally) from weight
gain of alligators fed 3% lysine (p = .058) (Figure 3). Weight gain of alligators fed 2.25% lysine
also was not significantly different from that of alligators fed 3% lysine (p > .999) or 3.75%
lysine (p = .414); however, weight gain of alligators fed 3% lysine was significantly less than
weight gain of alligators fed 3.75% lysine (p = .018) (Figure 3).
FIGURE 3
Body weight gain of American alligator (mean initial weight 53.3 ± 5.1 g) fed a graded series of lysine test diets for 326
days. Diets were formulated with corn gluten, menhaden fish meal, poultry byproduct meal, porcine blood meal,
menhaden fish oil, and a commercial vitamin and mineral premix used in manufactured alligator feeds. Diets provided
1.5, 2.25, 3.0, or 3.75% lysine as percentages of diet weight, as fed. Lines within the box plots indicate median (solid) and
mean (dashed) values. Median values of plots that share the same letter are not significantly different (p > .05)
Free lysine concentrations in blood were normally distributed (p = .165) but not of equal
variance (p < .05). One-way ANOVA on Ranks identified significant differences (p = .003) in
median free lysine concentrations among treatment groups. All pairwise multiple
comparisons indicated that free lysine concentration in blood of alligators fed 1.5% dietary
lysine was significantly lower than blood lysine concentration of alligators fed 3.75% lysine
(p = .006) but did not differ significantly from blood lysine concentrations of alligators fed
2.25% lysine (p = .484) or 3% lysine (p = .057) (Figure 4). Blood lysine concentration of
alligators fed 2.25% dietary lysine was not significantly different from that of alligators fed
3% lysine (p = .936) or 3.75% lysine (p = .057); nor was blood lysine concentration of alligators
fed 3% lysine different from that of alligators fed 3.75% lysine (p > .999) (Figure 4).
FIGURE 4

Concentrations of free lysine in blood of American alligator fed a graded series of lysine test diets for 326 days. Diets
were formulated with corn gluten, menhaden fish meal, poultry byproduct meal, porcine blood meal, menhaden fish oil,
and a commercial vitamin, and mineral premix used in manufactured alligator feeds. Diets provided 1.5, 2.25, 3.0, or
3.75% lysine as percentages of diet weight, as fed. Lines within the box plots indicate median (solid) and mean (dashed)
values. Median values of plots that share the same letter are not significantly different (p > .05)
4 DISCUSSION
The experiment reported here was conducted to investigate the effects of dietary lysine on
growth of captive-reared alligator fed compounded diets containing a range of lysine
concentrations similar to those reported in previous studies with aquatic species (Table 1).
We considered it possible that the dietary lysine requirement of American alligator might not
be similar to the requirements of fishes, crustaceans, or amphibians, which are not closely
related to crocodilians, whose closest living relatives today are birds (Nesbitt, 2011). Thus,
we considered it possible that lysine requirements of birds could provide another point of
comparison. Current recommended lysine requirements for use in feed formulation for
chicken, duck, goose, pheasant, quail, and turkey range 0.6–1.5% of the diet, with the
majority of requirements clustering around 1% of diet (Merck Veterinary Manual,
https://www.merckvetmanual.com/). These dietary requirements are similar to figures
published for some fishes (generally omnivores/herbivores) but tend to be lower than
requirements reported for most fishes and crustaceans (Table 1). This may be related, at
least in part, to the relatively high dietary energy requirements of homeothermic
metabolism in birds—that is, less protein but more energy needed per unit diet weight than
is required by poikilothermic animals like fishes and reptiles.
Unlike farmed poultry, many of the major farmed aquatic species, including the American
alligator, are carnivores in their natural environment. A dependence on animal protein in the
natural diets of carnivores would provide access to higher concentrations of dietary lysine
than would be available to omnivorous/herbivorous birds, which could affect the
development of a dietary requirement.
Reported amino acid requirements of some fishes, and a few crustaceans and amphibians
of aquacultural importance, suggest that a dietary concentration of 2–2.5% lysine appears to
be adequate for a variety of aquatic animals of commercial interest (Table 1). Results of this
study suggest that the lysine requirement of American alligator is also similar to
requirements reported for some other aquatic species (Table 1). Growth responses and
blood lysine concentrations indicate that compounded diets for American alligator should
contain at least 2.25% lysine (as fed), about 4.5% of dietary protein in this study, which is
within the range of requirements reported for other aquatic species, including some fishes,
crustaceans, and amphibians (Table 1).
In this study, we used measurements of alligator body length, body weight, and free lysine in
blood plasma to establish a first estimate of an adequate lysine concentration for a
compounded alligator diet composed primarily of practical feedstuffs available to
commercial feed manufacturers. Formulation of a low-lysine diet for free-feeding alligator is
challenging because many plant products with low lysine content tend to be unattractive
food sources. Although the American alligator can effectively digest and utilize plant
products in compounded diets (DiGeronimo et al., 2017; Reigh & Williams, 2013, 2018), diets
without animal protein supplements tend to be less readily accepted. The basal diet in this
study was designed to provide a relatively low concentration of lysine, from a plant protein
source, in a formulation sufficiently attractive to stimulate voluntary feed consumption,
which typically requires inclusion of animal protein supplements that contain higher levels
of lysine than plant protein products. The lysine concentration of the basal diet, which
contained three animal protein supplements in addition to corn gluten meal, was
approximately one-third higher than the lysine concentration of corn gluten meal alone and
was sufficiently attractive to be accepted by alligators.
Gains in body length and body weight did reflect significant differences among treatments,
but large variation in growth of individual alligators increased the difficulty of identifying
small differences among treatments. The unexpected result of no difference in median
weight gain among alligators fed 3% dietary lysine, relative to those fed diets containing one-
fourth less (2.25%) or one-fifth more (3.75%) lysine, appears to be due, at least in part, to
relatively large variation in growth response among individual animals within treatment
groups, perhaps due to differences in feed consumption. We have seen similarly anomalous
results in a previous alligator feeding trial (Reigh & Williams, 2018), which may be related to
agonistic behavior of more dominant animals reducing feed consumption of other
individuals. This could be addressed in future studies by identifying additional response
variables, beyond morphometric measurements, to improve estimates of dietary lysine
sufficiency.
5 CONCLUSIONS
Increases in body length, body weight gain, and free lysine level in blood plasma indicated
that a concentration of at least 2.25% dietary lysine—about 4.5% of protein in a 50% crude
protein diet—was adequate for growth of American alligator under the conditions of this
study.
ACKNOWLEDGMENTS
This research was funded in part by the Louisiana Department of Wildlife and Fisheries
(Agreement No. 2000186281). Additional support was provided by the Louisiana Agricultural
Experiment Station; the National Institute of Food and Agriculture, U.S. Department of
Agriculture, under Hatch project LAB94282; and by Cargill Inc.
CONFLICT OF INTEREST
The authors declare no conflicts of interest.
AUTHOR CONTRIBUTIONS
Robert C. Reigh and Millie B. Williams contributed jointly to the conception, design, and
conduct of this experiment; data collection and statistical analyses; and preparation of this
research article.
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2023-08-14 14:15 Growth effects of lysine in compounded diets for American alligator, Alligator mississippiensis - Reigh - 2022 - Journal

- Journal of the World Aqua…

Journal of the World Aquaculture Society / Volume 53, Issue 5 / p. 995-1005

APPLIED STUDIES Open Access    

Growth effects of lysine in compounded diets for American alligator, Alligator

Robert C. Reigh , Millie B. Williams

First published: 05 April 2022

Species Lysine requirement (% Source

2.2% in 44% CP diet Espe, Lemme, Petri and El-Mowafi (2007)

2.4% of diet NRC (2011)

Bullfrog (Lithobates 2.71% in 30.4% CP diet Mansano et al. (2017)

Common carp (Cyprinus carpio) 2.2% in 48% CP diet Nose (1979)

Species Lysine requirement (% Source

a Adapted in part from Nunes, Sá, Browdy and Vazquez-Anon (2014).

2 MATERIALS AND METHODS

2.2 Experimental design and dietary treatments

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3.0, or 3.75% lysine as percentages of diet weight, as fed

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Ingredient Diet 1 Diet 2 Diet 3 Diet 4

Ingredient Diet 1 Diet 2 Diet 3 Diet 4

Ingredient Diet 1 Diet 2 Diet 3 Diet 4

Protein 50.00 50.01 50.03 50.01

Lysine (% of diet) 1.50 2.25 3.00 3.75

Lysine (% of protein) 3.00 4.50 6.00 7.50

Lipid 12.45 12.42 12.40 12.38

Fiber 7.34 7.78 8.23 8.73

2.3 Statistical procedures

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Nevarez, J. (2007). Lymphohistiocytic proliferative syndrome of alligators (Alligator mississippiensis): A

Nijboer, J. (2020). Nutrition in reptiles. Merck Veterinary Manual. Retrieved from

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