Hatchling fitness in crocodilians is affected by “runtism” or failure to thrive syndrome (FTT) in captivity. In this study, 300 hatchling C. porosus, artificially incubated at 32°C for most of their embryonic development, were raised in semi-controlled conditions, with growth criteria derived for the early detection of FTT (within 24 days). Body mass, four days after hatching (BM4d), was correlated with egg size and was highly clutch specific, while snout-vent length (SVL4d) was much more variable within and between clutches. For the majority of hatchlings growth trajectories within the first 24 days continued to 90 days and could be used to predict FTT affliction up to 300 days, highlighting the importance of early growth. Growth and survival of hatchling C. porosus in captivity was not influenced by initial size (BM4d), with a slight tendency for smaller hatchlings to grow faster in the immediate post-hatching period. Strong clutch effects (12 clutches) on affliction with FTT were apparent, but could not be explained by measured clutch variables or other factors. Among individuals not afflicted by FTT (N = 245), mean growth was highly clutch specific, and the variation could be explained by an interaction between clutch and season. FTT affliction was 2.5 times higher among clutches (N = 7) that hatched later in the year when mean minimum air temperatures were lower, compared with those clutches (N = 5) that hatched early in the year. The results of this study highlight the importance of early growth in hatchling C. porosus, which has implications for the captive management of this species.
Citation: Brien ML, Webb GJ, McGuinness K, Christian KA (2014) The Relationship between Early Growth and Survival of Hatchling Saltwater Crocodiles (Crocodylus porosus) in Captivity. PLoS ONE 9(6): e100276. doi:10.1371/journal.pone.0100276
Editor: Richard Reina, Monash University, Australia
Received: February 8, 2014; Accepted: May 26, 2014; Published: June 24, 2014
Copyright: © 2014 Brien et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by a Holsworth Wildlife Research Endowment (ANZ Trustees Foundation), Northern Territory Research and Innovation Board student grant, and Charles Darwin University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Wildlife Management International Pty. Limited provided funding through the Rural Industries Research and Development Corporation. Wildlife Management International Pty. Limited also provided support in the form of salary for authors Matthew L. Brien and Grahame J. Webb, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.
Competing interests: Authors Matthew L. Brien and Grahame J. Webb are employed by a commercial company Wildlife Management International Pty. Limited. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.
Initial offspring size in the wild and in captivity can be expected to confer short to long term fitness advantages if it improves the ability to forage or capture food, avoid predation, compete with conspecifics, survive adverse environmental conditions      and ultimately produce more offspring  . This has been demonstrated in a wide range of mammals  , birds  , reptiles  , amphibians  , fish  , and arthropods   .
Large variation in offspring size and early growth rates are common within and between species  , between different populations of the same species   , and between siblings from the same clutch . Maternal size and condition  , genetic effects , multiple paternity, and conditions experienced prior to and after birth or hatching  may all be involved. With several species of mammals , snakes , fish , and frogs , the early nutritional environment is reportedly just as important as genetic influences in creating irreversible changes in growth rate and survival which affect long-term fitness    .
Despite larger offspring size often being correlated with higher rates of initial growth and survival (‘bigger is better’)     , there are many exceptions. There can be small or no effects of initial size on fitness   , skewed effects in which intermediate sized individuals are the most fit , or negative effects in which initial high growth rates are detrimental to fitness  . Among reptiles, the ‘bigger is better’ hypothesis appears to be generally supported    , but there are few data available for crocodilians in the wild or in captivity.
This study examines growth and survival in captive raised hatchling saltwater crocodiles (Crocodylus porosus), mostly from wild collected eggs (10 of 12 clutches). Average clutch size for C. porosus in Australia is around 50 eggs (range 2–78; 65.4 to 147.0 g eggs) producing hatchlings from 41.4 to 93.6 g  . In the wild an estimated 54% of hatchlings survive to 1-year-of-age  , whereas in captivity survival rates are higher, but vary greatly between establishments using different raising techniques . The primary cause of mortality in captivity (49% of all hatchling deaths in captivity) is ‘runtism’    , which is in essence a failure to thrive syndrome (FTT) involving voluntary starvation, which reduces immunity to disease and causes death between 70 and 200 days post-hatching   , with time to death dependent upon initial weight . The root causes of FTT in hatchlings remain poorly understood, but genetic  and incubation effects , elevated corticosterone levels , agonistic social interactions , various aspects of the raising environment (temperature, noise, visual stimuli) and management protocols (density, size disparity, disturbance) have all been implicated    .
The central aims of the present study were to determine whether growth trajectories established within the first three weeks post-hatching could be used as indices of short-term fitness. The degree to which size and body condition at hatching influences post-hatching growth is examined. Particular attention is focussed on clutch effects on both growth rates and the incidence of FTT. The FTT phenomenon in C. porosus and its implications on short-term fitness in captivity and in the wild are discussed.
Materials and Methods
This project was conducted under the approval of the Animal Ethics Committee of Charles Darwin University (permit no. A11003).
Clutches, eggs and incubation
Saltwater crocodile eggs and hatchlings used in these experiments were provided by Wildlife Management International (WMI; Darwin, Australia). There were effectively two groups of hatchlings, those clutches that hatched early in the year (16–24 January 2011; 5 clutches; N = 120) when ambient conditions were warmer, and those that hatched later in the year (29 March-22 May 2011; 7 clutches; N = 180) when conditions were cooler. Eggs came from wild nests (N = 10) collected 1–50 days after laying and captive nests (N = 2), collected 1–2 days after laying. Egg temperature within the nest (Tnest) was measured at the time of collection with calibrated thermometers, 2–3 eggs deep in the clutch. Daily fluctuations in Tnest are reasonably modest but peak at 19:00 h to 21:00 h . Measured Tnest and the time of measurement were used as a clutch-specific index for aligning what the mean (Tn.mean) and maximum (Tn.max) nest temperatures may have been up to the time of collection. Variation in egg size within clutches of C. porosus is low , and so mean egg size (mass, length, width) was measured from only 10 eggs per clutch. All eggs are carried within the oviducts of females prior to laying, and thus total clutch mass or volume is the best clutch-specific indicator of female size . The age of each clutch at the time of collection and the number of infertile eggs and eggs with dead embryos were estimated using methods described previously  .
Incubation to hatching was completed for all eggs at constant 32°C (±0.2°C) and 98–100% humidity, which produces hatchlings with the highest rates of growth and survival . Eggs were inspected regularly and the embryos of any dead eggs were used to determine whether death had occurred during incubation or prior to collection. Hatching typically occurred on the same day for each clutch. Hatchlings with deformities or which appeared to have excessive abdominal yolk, often resulting in lower survivorship, were excluded from the experiment. Sex was not determined, but 32°C is a male producing temperature, and the sensitive period for sex determination for the majority of eggs (10 of 12 clutches) occurred in the incubator   . For the two oldest clutches, sex may have been determined in the field. One (Tn.mean = 28.6°C at 50 days) was probably 100% female, whereas the other (Tn.mean = 33.3°C at 36 days) may have contained males and high temperature females    . All hatchings were held in the incubator (32°C) in crates for three days after hatching before release into their raising enclosures (day 4) and being fed.
Two types of experimental enclosures (initial and final) were used. Hatchlings were housed between days 4 and 24 in sibling-only groups of 7–10 individuals in the initial enclosures. They were box shaped (170×100×50 cm high) fibreglass enclosures with a land area (70×100 cm) that gradually sloped down to a water area (100×100 cm; ≤8 cm deep). At 24 days, hatchlings were transferred into the final enclosures, in mixed clutch groups of twenty individual hatchlings of similar size. The final enclosures were 3 m2 box-shaped concrete pens (150×200×150 cm high), with a land area (150×80 cm) that gradually sloped to a water area (150×120 cm; ≤19 cm deep). Each enclosure had a basking cage (100×120 cm) attached to the outside and accessible through an opening (20×10 cm) in the wall, which effectively increased the enclosure area from 3 to 4.2 m2. The cage increased the range of thermal options available to hatchlings. Hatchlings remained in the final enclosures up until a maximum of 10 months of age (300 days), but were sorted on the basis of size every 3–4 weeks   . Hence, density remained the same but the individuals in each final enclosure did not.
A “hide area”    was provided in all initial and final enclosures. Each was 80×90 cm, constructed of eight lengths (80 cm long) of 10 cm (diameter) PVC pipe strapped together in the horizontal plane and mounted on legs (5 cm). Hides were centrally positioned in the water (partly immersed) and overhung the land. One hide area was provided in the initial fibreglass enclosures, and two in each final enclosure. All hatchlings were subjected to a natural light cycle. Water temperature (Tw) was maintained at 31–32°C with thermostatically controlled injection of warm water (initial enclosures) or submerged heating pipes (final enclosures). Air temperature (Ta) averaged around 32–34°C but varied from 26–36°C at different times of the day depending on ambient temperatures. All animals were fed chopped red meat supplemented with di-calcium phosphate (4% by weight) and a multivitamin supplement (1%) at 16:00–17:00 h six days a week, with waste removed the following morning (08:00–09:00 h) when the water was changed. Equilibration of Tw after water changes took 0.5 to 1.5 hours.
Identification and measurements
A single uniquely numbered metal webbing tag (Small animal tag 1005-3, National Band and Tag Co.) was attached to the rear back right foot at the time of hatching. Snout-vent length (SVL in mm to the anterior of the cloaca) and body mass (BM in g) were measured when the animals were introduced into the initial enclosures at 4 days of age, at 24 days of age when transferred to the final enclosures, and again at 70 to 194 days of age (depending on hatch date; Data S1). All hatchlings were fasted the day prior to measurements being taken. Fasting for 48 hours prior to measurement does not affect growth rates but longer periods of fasting do . These data allowed a size-age curve to be constructed for each individual, from which, size at 90 days could be predicted, which avoided problems associated with the different real ages of individuals. These measurement intervals reflect previous indications that growth patterns established in the first few weeks and months are an important index of growth and survival after that time in crocodilians . Hatchling C. porosus that are afflicted by FTT can be expected to succumb to mortality from 70–200 days post-hatching , so although measurements were not taken after 70–194 days, mortalities were recorded up 300 days (10 months) after which survival rates tend to be 95–97% .
All statistical analyses were performed using JMP 8.0 statistical software . Where appropriate, data were checked for normality (Shapiro-Wilk's test) and homoscedasticity (Cochran's test) prior to statistical analysis. Morphometric relationships between egg length (EL) and egg mass (EM) of each clutch with SVL4d and BM4d; SVL, BM, and body condition (BC = BM/SVL g/mm) at 4 (SVL4d; BM4d), 24 (SVL24d; BM24d), and 90 (SVL90d; BM90d) days of age, and growth in BM between 4 and 24 days of age (GBM4-24d) and 24 and 90 days of age (GBM24-90d) were examined using regression analyses. Size at 90 days was predicted from the size-age relationship for each individual at 4, 24 and 70 to 194 days (dependent on actual age). As a check on biases associated with prediction, the actual BM90d and SVL90d of a sample of animals measured at 90 days (N = 48) were compared with the predicted values using paired t-tests. No significant difference was detected for the actual and predicted values of either BM90d (t = 0.26; df = 94; P = 0.79) or SVL90d (t = 0.56; df = 94; P = 0.58). We examined the effect of season (early: 16–24 January, N = 5; late: 29 March – 22 May, N = 7) on egg mass, hatchling size and growth (SVL and BM) at 4, 24, and 90 days, and %FTT using a PERMANOVA with clutch as a random factor nested within season. In PERMANOVA, probabilities that treatments are significantly different from each other are generated by permutation, which requires only limited assumptions about the distribution of the data: in particular, normality of the data is neither assumed nor required . The analysis was conducted with 1000 permutations in the PERMANOVA+ add-in for PRIMER . Regression analyses were also used to predict the probability of %FTT affliction up to 300 days from GBM4-24d and BC24d, and BM24d, using progress means (N = 20 animals). Unequal t-tests were used to examine differences in BM4d between hatchlings that became afflicted with FTT (N = 55) and those that survived (N = 245). A Pearson's chi-square test was used to examine the effect of clutch on the proportion of individuals that died from FTT affliction. The effect of clutch on size and growth of non FTT animals (N = 245) was analysed with an ANOVA. All means are reported ± one standard error with sample sizes.
Clutch, incubation and hatchling characteristics
The wild and captive laid clutches had different numbers of different sized eggs, which produced different sized hatchlings and came from different sized and aged females (indicated by total clutch mass). Clutches were collected at different embryo ages from nests with different temperatures that were laid at different times. Clutches also had different rates of infertility and embryo mortality before and during incubation, ultimately producing different proportions of apparently normal hatchlings (Table 1). The raising experiments also occurred at different times of year, and despite Tw being constant, Ta varied with the prevailing ambient temperatures.
Mean EM was highly clutch specific (Table 1), which in turn affected BM4d which is comprised of hatchling tissue plus the internalised residual yolk mass. Overall, there was a strong positive linear relationship between mean EM and EL of each clutch and BM4d but not with SVL4d (Table 2). However, mean clutch EM differed significantly between seasons (Table 2), with clutches of larger eggs laid earlier in the year (EM early = 116.86±3.05 g; late = 107.83±2.58 g).
Overall mean BM4d of C. porosus (N = 300) was 72.1±4.9 g (55.4–80.8 g), SVL4d was 144.5±3.8 mm (135–153 mm), and BC4d was 0.50±0.03 g/mm (0.39–0.50 g/mm). However, clutches of eggs laid early in the year produced hatchlings with significantly larger BM4d (75.09±0.38 g) than those produced later in the year (70.15±0.31 g; Table 3). However, this was not the case with SVL at 4 days. To examine the relationship between SVL4d and BM4d the data set was subdivided into <70 g (N = 86) and >70 g (N = 214) BM4d. There was no relationship between SVL4d and BM4d for hatchlings with a BM4d <70 g, while for hatchlings with BM4d >70 g, the relationship was linear (Table 2; Fig. 1a).
Relationship at a) 4d, b) 24d, and c) 90d for hatchlings born early (N = 120; blue) and late (N = 180; grey) in the year. BM90d was predicted from the size-age relationship for each individual at 4, 24 and 70 to 194 days.
At 24 days of age, the overall mean BM24d of C. porosus (N = 300) was 89.3±15.8 g (60–142 g), SVL24d was 159.6±7.0 mm (143–178 mm), and BC24d was 0.55±0.08 g/mm (0.41–0.80 g/mm). Clutches of hatchlings born later in the season were not significantly larger at 24 days than those born early in the year (Table 3). In contrast to the highly variable relationship between SVL and BM at 4 days, there was a much stronger relationship between BM and SVL at 24 days (Table 2; Fig. 1b).
Based on predictions at 90 days of age (N = 300), mean BM90d was 162.7±75.9 g (37–409 g), SVL90d was 187.7±24.8 mm (147–250 mm), and BC90d was 0.80±0.33 mm (range 0.25 to 1.62 g/mm). There were no significant seasonal differences in SVL90d or BM90d (Table 3). The relationship between SVL and BM at 90 days of age was strongly linear (Table 2; Fig. 1c).
Given the relatively uniform size of hatchling BM at 4 days (SD of BM4d = ±4.9 g) the individual variation in size by 24 days (SD of BM24d = ±15.8 g) and 90 days (SD of BM90d = ±78.6 g) was extreme and was reflected in BC. Mean GBM4-24d was 17.2±16.0 g but the range (−6.9 to 70.1 g) was already extreme with some individuals increasing by 70 g (+97.5%BM4d) while others had lost 7 g (−9.3%BM4d). Mean GSVL4-24d was 15.4±6.9 mm (range 1 to 30 mm). Mean GBM24-90d (63.7±67.1 g; range −40.2–278.6 g) and GSVL24-90d (24.2±17.91 mm; range −3 to 77) both increased substantially relative to the 4–24 day period, but variation remained extreme. There were no seasonal differences in SVL or BM growth (Table 3).
There was no significant relationship between BM4d and either BM24d, BM90d, or GBM24-90d (Table 2). However, BM4d did have a significant but highly variable relationship with GBM4-24d (Table 2), with higher growth among the smallest hatchlings born. Growth trajectories in BM and SVL established within the first 24 days were largely continued up to 90 days (Fig. 2; Table 2). A high proportion of individuals with the lowest GBM4-24d and GSVL4-24d and smallest BM24d and SVL24d failed to recover by 90 days (Fig. 2).
Relationship at 24 and 90 days: a) BM24d and BM90d, b) SVL24d and SVL90d, c) GBM4-24d and GBM24-90d, and d) GSVL4-24d and GSVL24-90d for hatchlings born early (N = 120; blue) and late (N = 180; grey) in the year.
Survival - FTT affliction
All animals which died during and after the study (<300 days post-hatching) were recorded. Of these, 55 (72% of mortalities) were seriously afflicted by FTT, did not respond to efforts to stimulate feeding, and died or were euthanized [31 (56.4%) at 70–100 days; 15 (27.3%) at 100–130 days; 9 (16.4%) at 130–202 days]. The remainder included animals (N = 17) that were otherwise healthy that died for other reasons between 90 and 300 days post-hatching. The proportion of individuals that died from FTT was not significantly different between seasons (Table 2).
BM4d was not significantly different between those hatchling afflicted by FTT (N = 55) and those that survived (N = 245; unequal t-test: t = −0.429; df = 298; P = 0.668). However, the probability of affliction with FTT was clearly indicated within the first 24 days, by the extent of growth in body mass (Table 2; Fig. 3a), body condition (Table 2; Fig. 3b), and body mass (Table 2; Fig. 3c). No affliction by FTT (0%FTT) was detected in animals that grew more than 8.2 g, achieved a BC24d of 0.55 g/mm SVL or a BM24d of 81.7 g in the first 24 days post-hatching. However, there were a total of 55 hatchlings that grew less than 8.2 g after 24 days and survived. These hatchlings grew significantly less (44.43±4.59 g; Welch's t-test: t = 7.49; df = 243; P<0.0001) between 24 and 90 days and were significantly smaller at 90 days (122.48±4.67 g; Welch's t-test: t = 9.82; df = 243; P<0.0001) compared with other hatchlings (GBM24-90d = 92.03±4.40; BM90d = 189.28±4.95).
Points are means for progress intervals (N = 20).
Among the non-FTT individuals (N = 245), clutch had a significant effect on BM4d, GBM4-24d, and BM24d (Table 4). As growth trajectories established within the first 24 days are continued to 90 days, clutch effects were also apparent in GBM24-90d and BM90d (Table 4). However, if the variance due to GBM4-24d is removed, no remaining clutch variation occurred in BM24d, GBM24-90d, or BM90d. This confirms that the clutch variation detected was mainly due to variation in GBM4-24d.
Across clutches, the mean incidence of FTT was 19.5+4.99% of hatchlings, but the range varied from 0% to 53.3%, demonstrating highly significant clutch effects (X2 = 48.36, df = 11, P<0.0001; Table 4). None of the clutch-specific variation in’FTT could be explained by the mean clutch and incubation characteristics (Table 1), although it was a relatively small sample (N = 12) and none of these variables were controlled.
Our results suggest that under similar experimental conditions, growth trajectories for the majority of C. porosus hatchlings established within the first 24 days post-hatching extend to 90 days and beyond. Similarly, individuals with a high probability of affliction by FTT up to 300 days post-hatching can be identified within the first 24 days by reduced growth. Therefore, instead of conforming to the ‘bigger is better’ hypothesis, hatchling C. porosus under these conditions appear to benefit from rapid early growth. However, whether this is the situation in the wild, where the environment is vastly different to that in captivity, is unknown.
While insights into the fitness of animals can be gained from both captive and wild animals, results need to be merged and assessed carefully. Growth and survival of neonate snakes (Thamnophis sirtalis) under captive conditions were similar to those in the field  . Yet other animals held in captivity can experience either greater or less fitness than their wild counterparts. Species which suffer high levels of stress  in captivity generally appear to be less fit, and this has been reported in certain species of lemur  , dolphin  , parrot  , and raptor , and predictably so if their ecology and response to humans is considered  .
For hatchling C. porosus under captive conditions, resources such as temperature, cover and food are abundant and there is no risk of predation . However, individuals are confined and forced to live at higher than natural densities, and are subject to human disturbance . In the wild, the availability of resources can often be limited or can fluctuate while the threat of predation is high and hatchling C. porosus must contend with larger crocodiles  . Female C. porosus also protect their offspring for the first few weeks and months post hatching  . As such, differences may exist in terms of which traits (size etc) may be selected for in captivity and in the wild, and this in turn may vary according to location and habitat.
For C. porosus, and many other crocodilians, there may be advantages in attaining a large size rapidly, in terms of the ability to avoid predation, compete with conspecifics, survive adverse environmental conditions, and reach sexual maturity . In the majority of cases, aggressive encounters between crocodilians favour the larger animal   , which then enables greater access to resources and subsequently improved long-term fitness both in the wild and in captivity  . Crocodylus porosus is considered the most aggressive and intolerant of conspecifics of all crocodilians , and agonistic behaviour begins within two days of hatching . Such behaviours are known to affect growth and survival in several species of reptile    , and this also appears to be the case in C. porosus under captive conditions   .
Clutch of origin and the incubation environment have been widely reported to affect post-hatching growth and survival in crocodilians      . Therefore, we tried to quantify sources of variation within the clutch, egg and incubation variables that may have biased our results (Table 1). None explained the variation in growth or affliction with FTT. However, the results highlight the inherent complexity of potential variables that may influence growth and survival, and the importance of assumptions about the homogeneity of neonates used for such raising trials  .
That FTT can be predicted after 24 days, suggests that the first few weeks post-hatching are crucial to short-term fitness of C. porosus under captive conditions with survival increasing up to 90% in individuals that increased in mass by 4–7g during this period. While this has been suggested for crocodilians by previous authors  , it has never been accurately quantified for any species. Regardless of whether this is the situation in the wild, it does suggest that if early conditions are unfavourable then short-term growth and survival can be compromised. This has been found in water pythons  in which different rates of growth and survival occur between years based on prey abundance during the early post-hatching stage.
The occurrence of FTT among captive-raised crocodilians is widespread, although because weakened animals are vulnerable to secondary illnesses, FTT may be under-reported . Regardless, C. porosus appear particularly prone to FTT affliction   . FTT is generally considered to result from an inadequate raising environment, although what constitutes an adequate raising environment for each species remains poorly understood and may be more species-specific than previously realised. For example, Alligator mississippiensis have substantially higher rates of growth and survival to one year of age when raised under identical conditions to C. porosus  . Hatchling A. mississippiensis are reported to initiate feeding more rapidly and on a wider range of food types, and as a species are considered far more tolerant of conspecifics with no or little aggression reported among juveniles in captivity    . Therefore, it is possible that the current approach to raising C. porosus in captivity, which was originally based on the model used for A. mississippiensis  , may be inadequate.
The extent to which FTT occurs in wild populations of C. porosus is not well understood, and would be difficult to quantify due to (presumably) an increased vulnerability of these weakened animals to predation. However, while emaciated or malnourished hatchling C. acutus , A. mississippiensis, and C. johnstoni (M. Brien pers. observation) have been observed in the wild on a number of occasions, hatchling C. porosus in an emaciated state have rarely been encountered in the wild  . Hence, FTT may not occur in wild C. porosus at anything like the rates reported in captivity . If so, genetic predispositions to FTT, which could be complicated by multiple paternity , may be a response to threats that can be avoided by appropriate behaviour in the wild, but not in captivity.
Factors that affect survival rates in hatchling C. porosus under captive conditions have clear implications on future growth and survival. However, it is not really clear that enhanced growth trajectories in the hatchling stage, forewarned in the first 24 days, will ultimately influence “fitness” of individuals in the long-term. It is unlikely that measured variation in growth within a time scale of 24 days will ultimately be correlated with variation in reproductive performance after a time scale of up to 20+ years  . This is because a completely different suite of factors dictate progress and outcomes during this time .
Variation in the survival and growth rates of C. porosus hatchlings in controlled environments are intimately connected to each other, particularly through FTT. Absolute growth, independent of hatchling size, is perhaps the best index of individual performance, which has implications for survival within captive environments, where the goal is often to enhance both survival and the early attainment of large juvenile size. However, it is important to realise that some hatchlings can recover from poor growth rates within the first 24 days (<8.2 g). Identifying and understanding the causes of FTT among hatchling crocodilians is essential for improving conservation and management programs aimed at raising crocodilians that are threatened or endangered for purposes such as head starting, in which individuals are released back to the wild at a size that ensures greater survival.
Individual size and growth data at 4 days, 24 days and predicted at 90 days for 300 hatchlings.
We thank Jemeema Brien and Charlie Manolis for their help in different phases of the project. We would also like to thank Wildlife Management International for the supply of animals, use of facilities, logistical support and major funding for this project. WMI funding through the Rural Industries Research and Development Corporation is gratefully acknowledged.
Conceived and designed the experiments: MB GW KC. Performed the experiments: MB. Analyzed the data: MB GW KM KC. Contributed reagents/materials/analysis tools: MB GW KM KC. Wrote the paper: MB GW KM KC.
- 1. Packard GC, Packard MJ (1988) Physiological ecology of reptilian eggs and embryos. In: Huey RB, Gans C, Pough FH, editors. Biology of the Reptilia. New York: Alan R Liss. pp. 523–605.
- 2. Congdon JD, Nagle RD, Dunham AE, Beck CW, Kinney OM, et al. (1999) The relationship of body size to survivorship of hatchling snapping turtles (Chelydra serpentina). Oecologia 121: 224–235. doi: 10.1007/s004420050924
- 3. Bronikowski AM (2000) Experimental evidence for the adaptive evolution of growth rate in the garter snake (Thamnophis elegans). Evol 54: 1760–1767. doi: 10.1554/0014-3820(2000)054[1760:eeftae]2.0.co;2
- 4. Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45: 341–369. doi: 10.1146/annurev.ento.45.1.341
- 5. Kissner KJ, Weatherhead PJ (2005) Phenotypic effects on survival of neonatal northern watersnakes (Nerodia sipedon). J Anim Ecol 74: 259–265. doi: 10.1111/j.1365-2656.2005.00919.x
- 6. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108: 499–506. doi: 10.1086/282929
- 7. Stearns SC (1983) The impact of size and phylogeny on patterns of covariation in the life history traits of mammals. Oikos 41: 173–187. doi: 10.2307/3544261
- 8. Gittleman JC (1986) Carnivore life history patterns: allometric, physiological, and ecological associations. Am Nat 127: 744–771. doi: 10.1086/284523
- 9. Grant PR (1986) Ecology and evolution of Darwin's finches. New Jersey: Princeton University Press. 476 p.
- 10. Wiggins DA (1991) Natural selection on body size and laying date in the tree swallow. Evol 45: 1169–1174. doi: 10.2307/2409724
- 11. Dunham AE, Miles DB (1985) Patterns of covariation in life history traits of squamate reptiles: the effects of size and phylogeny reconsidered. Am Nat 12: 231–257. doi: 10.1086/284411
- 12. Jayne BC, Bennett AF (1990) Selection on locomotor performance capacity in a natural population of garter snakes. Evol 44: 1204–1229. doi: 10.2307/2409283
- 13. Berger L, Uzzell T (1977) Vitality and growth of progeny from different egg size classes of Rana esculenta (Amphibia, Salienta). Zool Poloniae 26: 291–317.
- 14. Kaplan RH (1980) The implications of ovum size variability for offspring fitness and clutch size within several populations of salamanders (Ambystoma). Evol 34: 51–64. doi: 10.2307/2408314
- 15. Henrich S (1988) Variation in offspring sizes of poeciliid fish, Herandria Formosa, in relation to fitness. Oikos 51: 13–18. doi: 10.2307/3565801
- 16. Hutchings JA (1991) Fitness consequences of variation in egg size and food abundance in brook trout (Salvelinus fontinalis). Evol 45: 1162–1168. doi: 10.2307/2409723
- 17. Karlsson P, Wiklund C (1984) Egg weight variability in relation to egg mortality and starvation endurance of newly hatched larvae in some satryid butterflies. Ecol Entomol 10: 205–211. doi: 10.1111/j.1365-2311.1985.tb00549.x
- 18. Steinwascher K (1984) Egg size variation in Aedes aegypti: relationship to body size and other variables. Am Midl Nat 112: 76–84. doi: 10.2307/2425459
- 19. Marsh E (1986) Effects of egg size on offspring fitness and maternal fecundity in the orange throat darter, Etheostoma spectabile (Pisces: Percidae). Copeia 1986: 18–30. doi: 10.2307/1444883
- 20. Hutchings JA, Morris DW (1985) The influence of phylogeny, size and behaviour on patterns of covariation in salmonoid life histories. Oikos 45: 118–124. doi: 10.2307/3565229
- 21. McGinley MA (1989) The influence of a positive correlation between clutch size and offspring fitness, on the optimal offspring size. Evol Ecol 3: 150–15. doi: 10.1007/bf02270917
- 22. Madsen T, Shine R (2000) Silver spoons and snake body sizes: prey availability early in life influences long-term growth rates of free-ranging pythons. J Anim Ecol 69: 952–958. doi: 10.1111/j.1365-2656.2000.00477.x
- 23. Wilson PN, Osbourn DF (1960) Compensatory growth after under-nutrition in mammals and birds. Biol Rev 35: 324–361. doi: 10.1111/j.1469-185x.1960.tb01327.x
- 24. Jorgensen SE (1992) Development of models able to account for changes in species composition. Ecol Model 62: 195–208. doi: 10.1016/0304-3800(92)90091-r
- 25. Galatti U (1992) Population biology of the frog Leptodactylus pentadactylus in a central Amazonian rainforest. J Herpetol 26: 23–31. doi: 10.2307/1565017
- 26. Henry CJK, Ulijaszek SJ (1996) Long-term consequences of early environment: growth, development and the lifespan developmental perspective. Cambridge: Cambridge University Press. 255 p.
- 27. de Kogel CH (1997) Long-term effects of brood size manipulation on morphological development and sex-specific mortality of offspring. J Anim Ecol 66: 167–178. doi: 10.2307/6019
- 28. Birkhead TR, Fletcher F, Pellatt EJ (1999) Nestling diet, secondary sexual traits and fitness in zebra finch. P Roy Soc Lond B Bio 266: 385–390. doi: 10.1098/rspb.1999.0649
- 29. Maddox JD, Weatherhead PJ (2008) Egg size variation in birds with asynchronous hatching: is bigger really better? Am Nat 171: 358–365. doi: 10.1086/527500
- 30. Charland MB (1989) Size and winter survivorship in neonatal western rattlesnakes (Crotalus viridis). Can J Zool 67: 1620–1625. doi: 10.1139/z89-231
- 31. Sinervo B (1990) The evolution of maternal investment in lizards: an experimental and comparative analysis of egg size and its effects on offspring performance. Evol 44: 279–294. doi: 10.2307/2409407
- 32. Bobyn ML, Brooks RJ (1994) Interclutch and interpopulation variation in the effects of incubation conditions on sex, survival and growth of hatchling turtles (Chelydra serpentina). J Zool 233: 233–257. doi: 10.1111/j.1469-7998.1994.tb08586.x
- 33. Stamps JA, Mangel M, Phillips JA (1998) A new look at relationships between size at maturity and asymptotic size. Am Nat 152: 470–479. doi: 10.1086/286183
- 34. Bronikowski AM, Arnold SJ (1999) The evolutionary ecology of life history variation in the garter snake (Thamnophis elegans). Ecol 80: 2314–2325. doi: 10.1890/0012-9658(1999)080[2314:teeolh]2.0.co;2
- 35. McGehee MA (1990) Effects of moisture on eggs and hatchlings of loggerhead sea turtles (Caretta caretta). Herpetologica 46: 251–258.
- 36. Webb GJW, Buckworth R, Manolis SC, Sack GC (1983) An interim method for estimating the age of Crocodylus porosus embryos. Aust Wildl Res 10: 563–570. doi: 10.1071/wr9830563
- 37. Webb GJW, Cooper-Preston H (1989) Effects of incubation temperature on crocodiles and the evolution of reptilian oviparity. Am Zool 29: 953–971. doi: 10.1093/icb/29.3.953
- 38. Webb GJW, Manolis SC (1989) Crocodiles of Australia. Sydney: Reed Books. 160 p.
- 39. Isberg S, Shilton C, Thomson P (2009) Improving Australia's crocodile industry productivity: understanding runtism and survival. Rural Industries Research and Development Corporation, Project No. 9. pp. 4–147.
- 40. Buenviaje G, Ladds PW, Melville L, Manolis SC (1994) Disease-husbandry associations in farmed crocodiles in Queensland and the Northern Territory. Aust Vet J 71: 165–173. doi: 10.1111/j.1751-0813.1994.tb03381.x
- 41. Huchzermeyer FW (2003) Crocodiles: Biology, Husbandry and Diseases. UK: CABI Publishing. 337 p.
- 42. Garnett ST, Murray RM (1986) Factors effecting the growth of the estuarine crocodile, Crocodylus porosus, in captivity. Aust J Zool 34: 211–223. doi: 10.1071/zo9860211
- 43. Garnett ST (1986) Metabolism and survival of fasting estuarine crocodiles J Zool. 208: 493–502. doi: 10.1111/j.1469-7998.1986.tb01518.x
- 44. Turton JA, Ladds PW, Manolis SC, Webb GJW (1997) Relationship of blood corticosterone, immunoglobulin and haematological values in young crocodiles (Crocodylus porosus) to water temperature, clutch of origin and body weight. Aust Vet J 75: 114–119. doi: 10.1111/j.1751-0813.1997.tb14170.x
- 45. Brien ML, Webb GJ, Lang JW, McGuinness KA, Christian KA (2013a) Born to be bad: agonistic behaviour in hatchling saltwater crocodiles (Crocodylus porosus). Behav 150: 737–762. doi: 10.1163/1568539x-00003078
- 46. Webb GJW, Manolis SC, Ottley B, Heyward A (1992) Crocodile management and research in the Northern Territory: 1990–1992. In: Proceedings of the 11th Working Meeting of the IUCN-SSC Crocodile Specialist Group. Gland: IUCN. pp. 233–275.
- 47. Webb GJ, Messel H, Magnusson W (1977) The nesting of Crocodylus porosus in Arnhem Land, northern Australia. Copeia: 238–249.
- 48. Webb GJW, Manolis SC (1987) Methods for retrieving crocodilian embryos. In: Webb GJW, Manolis SC, Whitehead PJ, editors. Wildlife Management: Crocodile and Alligators. Sydney: Surrey Beatty and Sons. pp. 423–426.
- 49. Webb GJW, Beal MA, Manolis SC, Dempsey KE (1987a) The effects of incubation temperature on sex determination and embryonic development rate in C. johnstoni and C. porosus. In: Webb GJW, Manolis SC, Whitehead PJ, editors. Wildlife management: crocodiles and alligators. Sydney: Surrey Beatty and Sons. pp. 189–198.
- 50. Webb GJW, Manolis SC, Dempsey KE, Whitehead PJ (1987b) Crocodilian eggs: a functional overview. In: Webb GJW, Manolis SC, Whitehead PJ, editors. Wildlife management: crocodiles and alligators. Sydney: Surrey Beatty and Sons. pp. 417–422.
- 51. Webb GJW, Manolis SC, Whitehead PJ, Dempsey KE (1987c) The possible relationship between embryo orientation, opaque banding and the dehydration of albumen in crocodile eggs. Copeia 1987: 252–257. doi: 10.2307/1446070
- 52. Riese G (1991) Factors influencing the survival and growth of hatchling Crocodylus porosus in commercial crocodile farming. M.S thesis, University of Queensland.
- 53. Mayer R (1998) Crocodile farming: research, development and on-farm monitoring. Rural Industries Research and Development Corporation. Project No. DAQ-188A. 92 p.
- 54. Davis BM (2001) Improved nutrition and management of farmed crocodiles - hatchling to harvest. Rural Industries Research and Development Corporation. Project No. 01/123. 102 p.
- 55. Hutton JM, Webb GJW (1992) An introduction to farming of crocodilians. In: Luxmoore RA, editor. Directory of Crocodilian Farming Operations. Second edition. Gland: IUCN. pp. 1–39
- 56. SAS Institute (2010) JMP statistics and graphics guide. Cary, NC: SAS Institute Inc.
- 57. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: A Guide to Software and Statistical Analysis. PRIMER-E, Plymouth, UK.
- 58. Janzen FJ, Tucker JK, Paukstis GL (2000) Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles. J Evol Biol 13: 947–954. doi: 10.1046/j.1420-9101.2000.00234.x
- 59. Mason GJ (2010) Species differences in response to captivity: stress, welfare and the comparative method. Trends Ecol Evol 25: 713–721. doi: 10.1016/j.tree.2010.08.011
- 60. Petter JJ (1975) Breeding of Malagasy lemurs in captivity. In: Martin RD, editor. Breeding Endangered Species in Captivity. New York: Academic Press. pp. 187–202.
- 61. Lindberg DG, Berkson JM, Nightenhelser LK (1984) Primate breeding in zoos: a ten year summary. In: Ryder OA, Byrd ML editors. One Medicine. Berlin: Springer. pp. 162–170.
- 62. Connor RC, Wells RS, Mann J, Read AJ (2000) The bottle-nose dolphin: social relationships in a fission-fusion society. In: Mann J, Connor RC, Tyack PL, Whitehead H, editors. Cetacean Societies: Field Studies of Dolphins and Whales. USA: University of Chicago Press. pp. 91–125.
- 63. Couquiaud L (2005) Whales, Dolphins, and Porpoises: Presentation of the Cetaceans. Aquat Mamm 31: 288–310. doi: 10.1578/am.31.3.2005.288
- 64. Van Zeeland YR, Spruit BM, Rodenburg TB, Riedstra B, Van Hierden YM, et al. (2009) Feather damaging behaviour in parrots: a review with consideration of comparative aspects. Appl Anim Behav Sci 121: 75–95. doi: 10.1016/j.applanim.2009.09.006
- 65. Seibert LM (2006) Feather-pecking disorder in pet birds. In: Luescher AU editor. Manual of Parrot Behaviour. UK: Blackwell. pp. 255–265.
- 66. Kenward RE (1974) Mortality and the fate of trained birds of prey. J Wildlife Manage 38: 751–756. doi: 10.2307/3800041
- 67. Chamove AS, Hosey GR, Schaetzel P (1988) Visitors excite primates in zoos. Zoo Biol 7: 359–369. doi: 10.1002/zoo.1430070407
- 68. Lang JW (1987) Crocodilian behaviour: implications for management. In: Webb GJW, Manolis SC, Whitehead PJ, editors. Wildlife Management: Crocodile and Alligators. Sydney: Surrey Beatty and Sons. pp. 273–294.
- 69. Brien ML, Webb GJ, Lang JW, McGuinness KA, Christian KA (2013b) Intra- and interspecific agonistic behaviour in hatchling Australian freshwater crocodiles (Crocodylus johnstoni) and saltwater crocodiles (Crocodylus porosus). Aust J Zool 61: 196–205. doi: 10.1071/zo13035
- 70. Brien ML, Lang JW, Webb GW, Stevenson C, Christian KA (2013c) The good, the bad, and the ugly: agonistic behaviour in juvenile crocodilians. PloS one 8: DOI: 10.1371/journal.pone.0080872.
- 71. Carpenter CC, Ferguson GW (1977) Variation and evolution of stereotyped behaviour in reptiles. In: Gans C, Tinkle DW editors. Biology of the Reptilia, Ecology and Behaviour A. New York: Academic Press. pp. 335–554.
- 72. Phillips JA, Alberts AC, Pratt NC (1993) Differential resource use, growth, and the ontogeny of social relationships in the green iguana. Physiol Behav 53: 81–88. doi: 10.1016/0031-9384(93)90014-7
- 73. Goetz BGR, Thomas BW (1994) Use of annual growth and activity patterns to assess management procedures for captive Tuatara (Sphenodon punctatus). New Zeal J Zool 21: 473–485. doi: 10.1080/03014223.1994.9518017
- 74. Worner LLB (2009) Aggression and competition for space and food in captive juvenile tuatara (Sphenodon punctatus). M.S thesis, Victoria University. 111 p.
- 75. Webb GJW, Manolis SC, Ottley B (1994) Crocodile management and research in the Northern Territory: 1992–1994. In: Proceedings of the 12th working meeting of the Crocodile Specialist Group. Gland: IUCN. pp. 176–180.
- 76. Hutton JM (1987) Incubation temperatures, sex ratios and sex determination in a population of Nile crocodiles (Crocodylus niloticus). J Zool 211: 143–155. doi: 10.1111/j.1469-7998.1987.tb07458.x
- 77. Joanen T, McNease L, Ferguson MWJ (1987) The effects of egg incubation temperature on post-hatching growth of American alligators. In: Webb GJW, Manolis SC, Whitehead PJ, editors. Wildlife Management: Crocodile and Alligators. Sydney: Surrey Beatty and Sons. pp. 533–537.
- 78. Allsteadt J, Lang JW (1995) Incubation temperature affects body size and energy reserves of hatchling American alligators (Alligator mississippiensis). Physiol Zool 1995: 76–97.
- 79. Joanen T, McNease L (1976) Culture of immature American alligators in controlled environment chambers. P Wor Maric Soc 7: 201–211. doi: 10.1111/j.1749-7345.1976.tb00063.x
- 80. Mazzotti FJ, Bohnsack B, McMahon MP, Wilcox JR (1986) Field and laboratory observations on the effects of high temperature and salinity on hatchling Crocodylus acutus. Herpetologica 42: 191–196.
- 81. Webb GJW, Messel H (1977) Crocodile capture techniques. J Wildlife Manage 41: 572–575. doi: 10.2307/3800531
- 82. Messel H, Vorlicek GC, Wells AG, Green WJ (1981) Surveys of tidal river systems in the Northern Territory of Australia and their crocodile populations. Monograph No. 1. Sydney: Pergamon Press. 459 p.
- 83. Jamerlan ML (2002) Establishing mating systems by microsatellite analysis in declining saltwater crocodile (Crocodylus porosus) hatchling production at Edward River Crocodile Farm (Nth. Queensland). M.S thesis, University of Queensland. 118 p.
- 84. Ross JP (1998) Crocodiles: Status Survey and Conservation Action Plan. IUCN/SSC Crocodile Specialist Group. Switzerland and Cambridge: Gland. 135 p.
- 85. Chalfoun AD, Martin TE (2007) Assessments of habitat preferences and quality depend on spatial scale and metrics of fitness. J Appl Ecol 44: 983–992. doi: 10.1111/j.1365-2664.2007.01352.x