Crocodiles Are Large Reptiles

Published Date: 02 Nov 2017

1.0 Introduction

Crocodiles are large reptiles that are found throughout the tropical countries such as Africa, Asia, Americas and Australia. They are divided into the salt water crocodiles and the fresh water crocodiles. Their physical traits such as a streamlined body shape enables them to swim fast, with the assistance of a strong long tail (Cherkiss, et al., 2011). They have strong jaws that can crush even the strongest bone as it has been proven that crocodile bite force was the strongest. Their strong jaws enable them to grip on prey with the help of their numerous sharp teeth. Crocodiles are ambush hunters, which means that, their hunting behaviour was by observing and striking at the right time. As cold-blooded reptiles, their metabolism is slow (Rheyda, 2010). This is advantageous to them as they can survive long periods without food. The saltwater crocodiles and the freshwater crocodiles, shows a number of differences. The most obvious will be the habitat they live in. Saltwater will be around the sea in Northern Australia, Eastern India and Sri Lanka. They are also larger species in size (Kawamoto, 2006) and are also more aggressive. Their snout was longer with 14-15 sharp conical teeth (Sweeters, 2005), with armor plates on their neck area. On the other hand, freshwater crocodile’s distribution is restricted to Australia. This species is the smaller type of crocodile and is considered shy to humans. Their snout is shorter and slender with armor plates on their back which was absent in saltwater crocodiles (Tosun, 2013). Their body scales are also large and wider than the saltwater crocodiles. Both fresh and salt water expose the fourth tooth on the lower side of the jaw when the mouth was closed (Cherkiss, et al., 2011). The eardrums of these crocodiles are protected by flaps of skin where it was placed behind the eyes at the top of their head. Their nostrils are positioned at the end of their snout (Cherkiss, et al., 2011). All the features are located in suitable places to help the crocodile to breath, hear and see when submerged underwater. All crocodiles reproduce by oviparous method. They lay hard shelled white eggs. Their nests are made by dry plant materials or they dig pits (Tosun, 2013). The growth rate and maturity of crocodiles also depends on the temperature and the availability of food in the region. Although there is lack of data on thermal range in crocodiles (Hamann et al., 2007), the importance of water temperature and basking in crocodile’s behavior is becoming increasingly apparent (Campbell et al., 2010a). Finally, temperature was also shown by studies to influence the swimming ability of crocodiles (Elsworth et al., 2003).

This review focus on:

The diets of crocodiles

The effect of temperature on basking behavior of crocodiles

The locomotion activities of crocodiles.

2.0 Literature review

2.1 Crocodile Diets

The knowledge on diets of crocodilians is very important, as diet affects, behaviour, growth and its reproduction (Pauwels et al., 2003). This is because the diet explains much about predator-prey interactions, and also prey utilization among habitats (Rice, 2004). Crocodile diet depends on several factors, such as the habitat it lives in, the type of season which include climate season, reproduction season and also diet season, and finally, its body size and also sex. Fresh water habitat such as the mangrove swamp, river and lake or pond consists of different types of diet since the diet also depends on its habitat when compared to the sea or ocean (Rice, 2004). Crocodiles in winter period also tend to hunt larger types of prey as they provide more energy for them to survive the cold season. When fish was the most during their reproduction period, crocodiles will prey more on fish than other types of diets. On the other hand, if it was the time for an adult crocodile to reproduce, its diets mostly consist of prey with more calcium nutrients for its diets. And finally, as a crocodile grow larger, its jaws are bigger and also stronger. Thus, they are capable of preying on larger preys such as mammals and birds. Fresh prey in samples indicates that the crocodiles are feeding frequently (Rice, 2004).

The crocodile diet can be determined by observing what it eats, feeding trials on captive animals, biochemical and isotope analysis or as simple as obtaining samples of ingested food from its stomach as stated by Rice, (2004). Stomach content can also be obtained by post-mortem method. Since most crocodiles are endangered and threatened, a better and more ethical method was introduced. Non-lethal methods which fall into three categories were used in order to obtain the stomach content (Rice, 2004). First was the invasive scoops, that can mechanically retrieve material through esophagus, second, by irrigation methods that pumps water and flush material from the stomach out, or combination of both methods. This method was known as the hose Heimlich maneuver method. By using this method, it only cause very minor irritations at the esophagus, however, it was not a long lasting effect. Although this method was successful in giving good results, there was a minor disadvantage as it requires water under pressure. Thus the method was modified by adding a portable bilge pump or gas powered motor when no domestic water source is present (Rice, 2004).

Rice, (2004) used the Hiemlich manuever method. Sex and total length of capture crocodiles were determined. The captured crocodiles were held vertically head up. The crocodiles were then categorize into hatchlings (Tail length less than 30cm), juveniles (Tail Length equal to 30 and less than 90 cm), sub adults (Tail length equal to 90 and 180 cm), and adults (Tail length more than 180 cm) (Platt et al., 2000a).The crocodiles were also marked by clipping tail scutes in coded pattern. Later on, the hose Heimlich maneuver method was used to extract out all stomach content. The mouth of the crocodiles was then opened wide and a PVC tube with rubber band was then inserted into the crocodile mouth (Rice, 2004). A flexible hose 15mm coated with vegetable oil was then also inserted into the stomach and water was injected into the stomach of the crocodile. As the stomach of the crocodile was seen to expand, the crocodile was then inverted and the stomach of the crocodile was massaged (Platt et al., 2000b). The gentle massage at the stomach forces out the water together with its stomach contents. The process was repeated for several times until only clear water came out from its stomach. The stomach content was then treated with 10% formalin and 70% alcohol. Formalin is a chemical that prevents further digestion of the stomach content and also preserves it before further analysis (Rice, 2004).

The study results conducted by Agata, (2011) shows that diets of crocodile (Tomistoma schlegelii) are related to its body size. The diet included land invertebrates, plant materials and etc. The result from table 1 shows almost the same result as reported by Agata, (2011). From table 1, it shows that there are 18 crocodiles captured, with various tail length and body mass. Each crocodile was tagged with a number tag. The stomach content of the crocodile was examined and divided into 5 groups. Insects and Crustaceans will be the land invertebrates, Fish, Amphibians, Mammals and finally plants (Agata, 2011). From table 1, all 18 crocodiles, regardless of their body mass and tail length, their diet consists of land invertebrates. Land invertebrates found in their stomach content, proved that crocodiles regardless of body length and body mass feed on land invertebrates. Fish and plant materials are the second most diet consumed by the crocodiles from table 1. Since crocodiles are carnivorous animal, the plant materials that are found in most of the captured crocodile stomach contents was because of the crocodiles indirectly consuming it or secondary consuming when hunting for preys (Agata, 2011). Amphibians are rarely a popular diet among crocodiles, as it was only found in 1 of the capture crocodile stomach. Finally, mammals are only found in stomach content of crocodiles with body mass 1900 and above of the captured crocodiles. This proves that, as crocodiles grow larger, they are more capable of preying on a wider range of diet as their jaws gets bigger with a stronger bite force (Alejandro, 2008). In some studies, domestic mammals such as goat, cows and even dogs are potential prey for these adult crocodiles (Akhilesh et al., 2012). Mammals were not found in crocodiles that had 1900gm body mass and below. This proves that crocodiles are opportunistic feeders as they feed on a wide range of prey (Agata, 2011).

Investigation of Alejandro, (2008) also shows that crocodile (Crocodylus acutus) diets are also related to body size and sex. The examination method used was the same as Agata, (2011). Table 2 categorizes crocodiles into sex, the male and female with various total lengths. Regardless of sex and body length, the main diet for all the captured crocodiles consists mostly of fish. Their second most important diet was the crustaceans. In a study carried out by Akhilesh et al (2012), same results were obtained with smaller juvenile salt crocodiles that are restricted to smaller animals such as fish and crustaceans. Fish and crustaceans were more to female’s crocodiles. The least popular diet among the crocodiles were the insects, as it shows a very small percentage in the stomach content of the captured crocodiles (Table 2). Insects are also indirectly consumed or secondary consumed as the results of Agata, (2011) shows no insect in stomach content. Mammals are also only found in the stomach content of larger groups of crocodiles with total length of 140mm and above. Finally mammals are only found in the larger males stomach (Alejandro, 2008).

Alejandro, (2008) shows the stomach content percentage of various diet in recapture crocodiles (Table 3) from the previous table 2 captured crocodiles. There were 4 recaptured crocodiles, consisting of 3 females and 1 male. From the table 3, again it shows that, juvenile and sub adults crocodiles diet consist of mostly primary diet fish and secondary diet crustaceans even after recapture. Their diets remain the same since their captured period. Insects were also the least consumed as they may be indirectly or secondary digested. While for the larger female, during the captured period, its stomach content contained mostly of crustaceans which was 99% and only 1% insect (Alejandro, 2008). Insect was secondary consumed or indirectly consumed by it, thus concluding that during the captured period, this large adult female prey only on crustaceans. While during the recaptured period, their crustaceans diet dropped to 20 percent and with 79 percent of mammals. Finally the diet of largest male crocodile consisted 100 percent of only bird during the capture, and also after recapture. It also proves that only larger crocodiles prey on mammals and only birds. Mammals were found in the male. Male has larger TL then female (Alejandro, 2008). As crocodiles grow larger, they are potentially able to prey on a wider range of diets with the help of their large and powerfully developed jaws (Alejandro, 2008).

From these studies carried out by Agata, (2011) and Alejandro, (2008), crocodiles show ontogenic shift in prey choice (Borteiro et al., 2009). It can be concluded that fish are the primary main diet of crocodiles since fish diversity was relatively high in wetlands system. And birds are only found in adult male crocodiles. As crocodiles grow larger, the diet varies to a wider range with mammals and birds. Alejandro, (2008) also found that C.acutus prey mainly on fish, mammals and birds. The difference will be the consequences of jaw development, providing an increase in possibility of diet diversification, giving them the capacity to prey on larger and wider prey. With their strong jaw and sharp teeth, crocodiles tear larger prey by rolling their body and later on leaving their larger prey to decompose and consume later (Stickney, 2000). But the result that was obtained by Borteiro et al., (2009), was doubted since the method used to determine the stomach content was by feces analysis. Similar results were shown by (Vanweerd, 2010) in Crocodylus mindorensis where same diets such as land invertebrates and small fish were found in stomach content of juvenile crocodiles while birds, snakes and pigs were found in adult stomach content. Adult females from Alejandro, (2008) showed that it consumed almost 99 percent of crustaceans as diet. This finding was because during the reproduction period of crocodiles, they need more calcium minerals in order for them to produce clutches of eggs. Wallace et al., (2008) studies also proved that they consume carrion. The rate of growth of crocodiles varies with food availability and also the temperature. According to (Cherkiss, et al., 2011), effective digestion for crocodiles occur correctly only when the body was in a certain temperature range. In some studies, crocodiles have been proven to feed less during hot day and that cooler temperature decreases the rate of digestion. The purpose was that the crocodiles can conserve energy more effectively (Marin, 2007). As stated by Somaweera et al., ( 2011) in his study, the prey or diets for crocodiles were also affected by the habitats it inhabits. Study conducted by Somaweera et al., ( 2011) shows that the prey availability in an area was directly proportional to the concentration of crocodiles in the habitat area. This was especially true for hatchling crocodiles that maximize their food intake with less exposure to potential predators. A favourable habitat for hatchling crocodiles will be the float mat area, where the water was covered by some plant materials. This was because, such habitat provides benefit features, more prey availability and less exposure to threat. Adult crocodiles are able to feed in exposed area since the potential predator for adult’s crocodiles are lesser and successful hunt by adults crocodiles are greater. In the study by Somaweera et al., (2011), in open area habitats, the prey availability was less compared to the grass area habitat or the float mat habitat. The highest prey availability will be the grass habitat area. However, the amount of food intake for all crocodiles was very similar regardless of the concentration of prey availability in different habitats. This result shows that, although with prey availability in certain habitat, the amount of food intake was constant. The lower amount of diversity of prey items consumed in areas which are lower in food concentration were balanced with food intake with higher mean mass per prey item as stated in Somaweera et al., ( 2011) study. The types of diets present were land invertebrates and small fish which are abundant in float mat area, suitable for hatchling crocodiles. While, for adult crocodiles, diets consists of large mammals which are commonly found in grass area or open habitat area (Somaweera et al., 2011).

Table 1: Analysis of stomach content of captured T. schlegelii.

(Agata, 2011)

Table 2: Percent volume of food items in stomach contents of Crocodylus acutus

(Alejandro, 2008)

Table 3: Percent volume of food items in stomach contents of captured (c) and recaptured ( R) Crocodylus acutus

(Alejandro, 2008)

2.2 Role of temperature on basking behaviour

Basking behaviour of crocodiles is very important for them in maintaining their body temperature at favourable state. This behaviour is known as thermoregulation. During the activity, crocodiles will utilize its microhabitats that encompass both terrestrial and aquatic environments and a variety of behavioural postures (Grigg et al., 2001). The main reason why crocodile thermoregulate is to increase their body temperature for daily optimum activity performance and also to aid food digestion which also requires a certain temperature. Example for their daily activities such as swimming and hunting for prey, the basking activity of crocodiles usually starts every morning to the late afternoon period (Grigg et al., 2001). The basking activity of crocodiles can be either be shuttling between the land and water, or half portion of the body submerged and half of it on shore which is known as pre-bask. If the crocodiles are seen on the surface of the water, it was known as surface bask where no movement was observed. Normal basking was where the crocodile was fully on shore and no movement at all (Venugopal et al., 2003). It can also be shuttling between area which are shaded or area that are direct expose to sun. The basking activity in the morning was so that towards the night period, crocodiles can be very active (Stafford et al., 2000). When active, crocodiles extend most of their energy and it needs several hours to regain back. Crocodiles basking activity sometimes aids with gaping which is the same as panting in dogs. This behaviour was seen to be absent in the alligator. This was because only crocodiles had large number of sweat glands on their tongue. Moreover, basking behaviour of crocodiles was affected by the habitat they stay and also its environmental temperature such as the wind velocity, water temperature, soil temperature and the season (Grigg et al., 2001).

Downs et al., (2008) reported that Crocodylus niloticus starts basking activity around 10.00 hour irrespective of body size and sex. The method used by Downs et al., (2008) was that all captured crocodiles were immobilized using galamine trithiodide. The crocodiles are now paralyzed and are not able to move. And surgery was conducted on the captured crocodiles. The surgery was done carefully under sterile condition. Local anesthetics were infiltrated into the site of incision. Later on, 2 Thermochrome iButtons dataloggers with 0.5 precise were implanted into subcutis of crocodiles. The Thermochrome ibuttons dataloggers will record temperature of the crocodile for every 20 minute. The crocodiles were then kept under cool condition after the surgery before releasing. Few Thermochrome ibuttons dataloggers were also placed at different areas to test the surrounding ambient water temperature, soil and surrounding air temperature (Downs et al., 2008).

Table 4 by Downs et al., (2008) shows 4 captured crocodiles with 2 males and 2 females. All 4 are different in total length. From table 5, which was also by Downs et al., (2008), all 4 crocodiles started basking at minimum temperature around 8.00 hour. The maximum time of basking was around 14-15 hour for all 4 captured crocodiles. The minimum mean body temperature of 4 captured crocodiles was around 18-19 degree Celsius. The body temperature of all 4 crocodiles rose as their basking activity started. The maximum mean body temperature of the 4 captured crocodiles was around 26-29 degree Celsius (Downs et al., 2008). Finally the table shows the optimum basking temperature for the Nile crocodile was in between 26.9 to 29.2oC. While the minimum optimum temperature for a crocodile to carry out its optimum daily activity and to survive will be 18.8-19.6 (Downs et al., 2008).

Results of experiment conducted by Downs et al., (2008) as shown in figure 1, shows that the heating rate for the 4 captured crocodiles body temperature increases rapidly compared to the cooling rate of body temperature. From the 9 hour, the heating rate of all 4 crocodiles showed a rapid increase until it reached the 14 hour of the graph, which was the maximum. It then decreased steadily after the 15 hour until the 8 hour which was the minimum body temperature. The mean maximum temperature of 4 crocodile was at 27-29 degree Celsius according to the graph, while the minimum optimum temperature for crocodiles to survive and carry out daily activity was around 19 degree Celsius (Downs et al., 2008).

Figure 2 by Downs et al., (2008) shows that the soil temperature was higher when compared with the air back pen and air tree temperature. Although they are little differences in temperature, all 3 of them show that the heating rate was also faster when compared to their cooling rate. All 3 temperatures also rises starting at 7 hour but only the soil temperature reached maximum slightly later compared to the other 2 air temperatures, and thus the soil maximum temperature was higher. Both air temperatures reached maximum in between 12-13 hour and in between 23-24 maximum degree Celsius. The soil temperature reaches maximum at the 14 hour about 27 degrees Celsius. And finally, all 3 decrease at the 15 hour, until it reached the minimum temperature about 15 degrees Celsius at the 6 hour (Downs et al., 2008). On the other hand, figure 3 from Downs et al., (2008) study shows 3 types of water temperatures. The results show a slow and steady increase in temperature and also a steady and slow slope decreasing rate of temperature in all 3 types of water temperatures. Overall, all 3 water temperature did not increase much throughout the day and also did not decrease much around 16.5-20.5 degree Celsius. All three water temperatures also started to increase around the 8 hour and reach maximum temperature which was in between 19-20.5 degree Celsius at the 14 hour. All 3 then decreased after the 15 hour until the 7 hour (Downs et al., 2008).

When comparing figure 2 and 3 from Downs et al., (2008), crocodiles prefer to bask at soil then in water since the ground temperature was obviously greater than the water temperature during the basking period which was at the 9 to the 15 hour. By doing so, the crocodiles can bask with the most minimum effort, as the temperature from the soil can be easily conducted to the body core of the crocodile, and thus increase the temperature at a faster rate. If the crocodile stays in the water during the basking period, the water will act as an insulator to heat, and the maximum temperature reached by the crocodile was not favourable. Similar results were obtained by Matthew et al., (2012) in Crocodylus porosus (Downs et al., 2008).

From figure 4, Matthew et al., (2012) study shows that the body temperature of captured crocodile rises as the sun rises. Since it was during the summer period, crocodile’s body temperature tends to increase slightly earlier at 8 or 9 hour. And they quit basking at late afternoon. The horizontal line on figure 4 indicates the mean value across all hours. At the middle of the horizontal line, the heavy bar indicates the quiescent period (Matthew et al., 2012). Quiescent period was the period when the crocodiles were inactive or only showed a bit of movement. The quiescent period was in between 11-16 hour. The quiescent period from figure 4 also shows the greatest body temperature of crocodiles. Out of the heavy bar, will be the non-quiescent period, where the crocodiles were active, and their body temperature decreased at 17-10 hour period, which was at night when crocodile was not basking (Matthew et al., 2012). From figure 5, it shows the movement per hour of crocodiles during each hour. As shown in figure 5, the least movement was during the quiescent period when the crocodiles were basking. The inactive movement of crocodile was to make sure that they conserve more energy, and prevent heat from losing faster during their night hunting or swimming activity. The hunting period was at night starting at the 19 hour of figure 5. As shown on figure 5, the movement per hour of crocodile reaches 10 movements per hour during the non-quiescent period (Matthew et al., 2012). The general daily cycle in this study of body temperatures was less pronounced, but it was almost similar with that reported for sub adults and adults of several crocodilian species in nature (Downs et al., 2008).

Figure 6 done by Venugopal et al., (2003) showed quite similar results. Throughout the 6 weeks, the number of crocodiles seen basking started to increase after the 8 hour. The most number of crocodiles seen basking was during the second week, where it reaches the highest mean number about 16.00 at the 11 hour time. Not only the second week, the other 5 weeks also show the maximum mean number of crocodiles basking during the 11 hour time (Venugopal et al., 2003). While the lowest mean number of basking activity was in between 0 to 4 at the 7 hour. After the morning basking period, at late afternoon the 16 and the 17 hour, week 1 to week 4 showed an increase in mean number of basking crocodiles, in fact higher than the mean number during the morning. While on the fifth and the sixth week, the mean number of basking crocodile’s decreased after the 11 hour (Venugopal et al., 2003).

Figure 7 by Venugopal et al., (2003) shows the different sizes of Crocodylus palustris basking at different time intervals. During the first hour period, 7- 9.59 time, juvenile crocodiles had the highest percentage among the other size classes. The percentage was about 60 percent of the basking activity while sub adults showed about 20 percent and adults only 10 percent. The number of juvenile crocodiles seen basking is getting less as after the 9.59 hour time. But during the 10 hour time, the number of sub adults crocodiles and adults seen basking increases where the juvenile crocodile percentage got lower (Venugopal et al., 2003). The percentage of sub adult crocodiles increases until 40 percent while the adults crocodiles increase until 30 percent. The juvenile crocodiles were the lowest at 20 percent only. At the third period time, in between 13 hour to the 14.59 hour time, the percentage of juvenile crocodiles were the lowest among 1 day time. The percentage of the juvenile crocodiles was below 10 percent, while the sub adults and adults exhibited a percentage greater than the juvenile crocodiles at 30 percent. And finally at time 15 to 18 hour, adult crocodiles were the most among 3 classes of crocodile, about 24 percent, while the lowest, juvenile crocodile less than 10 percent (Venugopal et al., 2003).

From the results from Downs et al., (2008) crocodiles showed similar pattern to other reptiles. Their body temperature easily increases rapidly but the cooling rate of the body will be much slower. Results obtained by those studies, show not much a difference between the mean temperature in both species and the basking period was almost the same which was around the 10 hour. Almost similar results Venugopal et al., (2003) showed that the basking period of crocodile started by the 8 hour and the 11 hour. This slight difference could be due to several factors such as, the season in the studies. The shift in thermoregulatory behaviour and also the preferred body temperature of crocodiles clearly indicates that the crocodiles are able to sense their environment surroundings. This shows that, there was an integrated response in between biochemical compensation and the crocodile’s behaviour (Glanville et al., 2006). During the summer period, crocodile tend to bask slightly later when compared to winter. Similar results were also shown by Venugopal et al., (2003) studies, where he stated that crocodiles tend to bask slightly later during an extreme hot day as they spend most of their time submerged. While their basking period will slightly end faster too when compared with winter period. This was because that, during summer period, the surroundings temperature was higher and it was a suitable condition for the crocodiles to achieve optimum temperature with the least effort needed. The heat can be obtained from the heated soil which is directly conducted to its body core. Land basking in crocodiles occur as the air temperature of the surrounding was greater than the water temperature (Venugopal et al., 2003). Other than that, during rainy season, or may be rainy day, crocodiles tends to stay longer in water and only emerged to land at a later period to bask, usually later than 10:00 (Downs et al., 2008). This was also because that the outside condition will be not favourable as the temperature varies differently and are much lower. As stated by Franklin et al., (2003), the crocodile’s amphibious lifestyle has a significant influence on rate of heat gain and also loss due to the markedly different thermal characteristics of water and air. The strong wind during rainy day will also cause heat lost faster than heat gain during the basking period. This was also aided by the wet soil which also cause crocodiles hard achieve its favourable body temperature. In other words, the water can act as a heat source or a heat sink depending on the condition and environment outside (Downs et al., 2008). The changes in basking behaviour of crocodiles in respect to time spent and time of day are season dependent (Venugopal et al., 2003). On the other hand, juvenile crocodiles tend to bask earlier than usual and also quit basking as sub adults and adult crocodiles start basking. This was because as several studies had shown that they need to avoid the interactions with dominant larger individuals (Venugopal et al., 2003). It was also stated by Venugopal et al., (2003) that larger crocodiles require basking for a longer period of time. Endothermic mammals on the other hand, regulate their body temperature very narrowly. Departure from that narrow range often resulted in death of the animal (Harjunpää et al., 2004).

Table 4: Sex and length of Nile crocodiles from which body temperature was obtained

(Downs et al., 2008)

Table 5: Summary of 4 Nile crocodiles mean minimum and mean maximum body temperature at what time period.

(Downs et al., 2008)

Figure 1: Mean hourly change in temperature of Nile crocodile during winter

(Downs et al., 2008)

Figure 2: Meanly hourly change in air and soil temperature when crocodiles body temperature was measured.

(Downs et al., 2008)

Figure 3: Meanly hourly change in water temperature when crocodile’s body temperature was measured.

(Downs et al., 2008)

Figure 4: Mean hourly change in temperature of Crocodylus porosus during summer. Horizontal line indicates mean value across all hours and heavy bar indicates quiescent period (QP).

(Matthew et al., 2012)

Figure 5: Activity of Crocodylus porosus in a thermal gradient. Horizontal line indicates mean value across all hours and heavy bar indicates quiescent period (QP).

(Matthew et al., 2012)

Figure 6: The mean number of Crocodylus palustris basking at each hour during 6 weeks.

(Venugopal et al., 2003)

Figure 7: Proportion of Crocodylus palustris of different sizes observed basking at

different time intervals.

(Venugopal et al., 2003)

2.3 Locomotion activities of Crocodiles

The locomotion of crocodiles mostly consist of swimming and diving. These are very essential and it is directly linked to their performance since it affects the animal’s ability to capture prey, avoid prey and to migrate (Grigg, 2001). The energy cost for crocodiles in swimming are directly related to its body shape and swimming mode. The energy cost will be high in semiaquatic crocodiles then other fully aquatic animals (Frey et al., 2001). In the case of swimming, the movement can be significantly be affected by the motion of the fluid water in which they are immersed in (Alerstam et al., 2003). Swimming animals include crocodiles adapt to the flows of water by 2 responses which are different, but not mutually exclusive type of response. First response, they can move in times or swimming-depths so as to coincide with the flow which are more favourable with their preferred direction. Secondly, they can compensate for any drift away from their goal method to maximize the distance covered (Jason et al., 2011). For example, the estuarine crocodile (Crocodylus porosus) shows selective tidal stream transport behaviour during long distance river travel events. Meaning that, they swim in surface water currents when it is favourable to their direction and dive to the river bed or climb out of the bank when in contrary (Jason et al., 2011). It was also stated by Jason et al., (2011) that crocodiles are incapable of prolonged bouts of sustained swimming, thus their movement consists of active downstream and passive downstream transport (Elsworth et al., 2003). Crocodile’s sustained swimming performance, often measured as the maximum sustainable swimming speed (Ucrit) which is much poorer in animals such as semiaquatic crocodiles then wholly aquatic animals such as fish (Plaut, 2000). Thus the swimming performances for crocodiles are a greater ecological than terrestrial locomotion, since crocodiles do not possess the ability to aquatically respire and to remain submerged for a long period of time compared to similar small sized endotherms (Brischoux et al., 2008). Furthermore, crocodiles are categorized as the most social type of animal among other reptiles. Crocodiles often show sustained activity during mating. For crocodiles, their metabolic rate was only 10-20% that of larger mammals similar in body size. This shows that they are able to remain submerged for longer periods than those endothermic animals with similar body size (Franklin et al., 2009). In terms of crocodiles, mass scales are isometric with oxygen stored and also metabolic rate scales with allometric component are less than 1 (Wallace et al., 2008). In order to sustained their swimming performance, crocodiles need to depend on their body size and also its surrounding temperature. While crocodiles are swimming, the water current which opposes them will slow them down and eventually tires them as they continue to swim. Crocodiles need more energy in order to overcome the water current. And thus it was known as sustainable swimming speed (Wallace et al., 2008).

Elsworth et al., (2003) results showed the effect of body size and temperature in swimming performance of Crocodylus porosus. The method used in this study was that few juvenile crocodile, species Crocodylus porosus were acquired from a commercial zoo. The crocodiles were then placed in an oval-shaped swimming flume. The oval-shaped swimming flume was specially designed so that its water speed and the water temperature can be remotely controlled. The temperature of water inside the oval-shaped flume was controlled by a heater. And the water speed was controlled by 2 propeller build in the swimming flume. The crocodiles were then observed. All observations were recorded.

Elsworth et al., (2003) conducted an experiment to show the effect of body length of crocodiles on its critical swimming speed at different water temperatures as shown in figure 8. It was obvious that at higher temperature, which was 33 degree Celsius, the crocodile’s critical swimming speed was greater compared to the cooler temperature. A crocodile with body length 90cm can reach a maximum critical swimming speed at 65 CMs-1. For a smaller crocodile with body length 30cm, the maximum critical swimming speed is to be 30 CMs-1 (Figure 8). These results were obtained at 33 degree Celsius. While for 18 degree Celsius, all crocodiles in different body length showed lower maximum critical swimming speed compared to 33 degree Celsius. As the body length of crocodile increased, the critical swimming speed also increased (Elsworth et al., 2003). This was due to larger crocodiles having greater body muscle mass compared to smaller ones. The crocodiles are able to generate more energy to overcome the opposing tide water, thus also able to swim at a faster rate. Elsworth et al.,(2003) , study results on length specific Ucrit was shown in figure 9 , which was the amount of time a crocodile, able to continue swimming at the same speed before it stops (Plaut, 2000). The greater the body length of the crocodile, the lower its length specific Ucrit BLs-1 value. For the smallest size crocodile of 20cm, it shows that the length specific Ucrit BLs-1 value was the highest compare to the large size crocodile. Regardless of both temperature, the smaller size crocodile still shows the greatest length specific Ucrit BLs-1 (Elsworth et al., 2003) The crocodile around 90cm body size showed less length specific Ucrit BLs-1 about 0.4 compared to the smallest 20cm size at 18 degree Celsius condition while 33 degree Celsius condition will be around 0.6. This directly shows that temperature of water also effect the length specific Ucrit BLs-1 as higher temperature length specific Ucrit BLs-1 shows greater value compared to the cooler temperature length specific Ucrit BLs-1. The reason behind it was because that larger size crocodiles will have larger surface area compared to smaller sized crocodiles. Having larger surface area will have more difficulties in overcoming the water tide forces as it opposes the direction of the swimming crocodile (Elsworth et al., 2003). Thus muscle will easily get fatigue as more acetic acid accumulates. Figure 10 then shows the relation between water temperature and length specific Ucrit BLs-1 with relative to difference body size. From the figure 10, we can see that thereis no activity at 15 degrees Celsius for all 3 size classes of crocodiles. As the temperature rises slightly, the length specific Ucrit BLs-1 increases rapidly until it reaches 0.4 for medium and large size class. The small size class shows greater result compared to both larger sized classes which was almost 0.6. The length specific Ucrit BLs-1 was quite constant in between 17-33 degree Celsius. Above 33 degree Celsius, include the smaller size class crocodile, all 3 size classes decreases rapidly its length specific Ucrit BLs-1 value. This shows that the crocodile was not able to cope at temperature higher than 33 degree Celsius. Overall, crocodiles that are larger in size, in suitable temperature was able to swim at a faster rate, but it will only last for a short period due to larger body surface are (Elsworth et al., 2003).

Hamish et al., (2010 a) stated that diving in crocodiles are categorized into two types of dive. The first dive was known as the resting dive. Resting dive was the type of dive, where crocodiles stay for a long period of time under water, fully submerged and only rises to pay its oxygen debt. During resting dive, the crocodiles showed zero movement at the bottom or the least movement. On the other hand, active dive was the dive where crocodiles dive for only a short period of time (Seebacher et al., 2005). It may be fully submerged or partially submerged at the surface of the water. Active dive was usually associated with swimming, meaning that crocodiles undergoing active dive shows great movement, usually for hunting and swimming activity. Moreover, for both diving activities, both are affected by its physiological condition, ecological and environment effect, and finally their response to treat (Hamish et al., 2010 a).

Hamish et al., (2010a) study shows ecological and physiological determinants of dive duration in Crocodylus johnstoni. From the study by Hamish et al., (2010a), the method used was that crocodile’s species Crocodylus johnstoni were captured. The crocodile’s total length and their body mass were measured and recorded. A time depth recorder was attached at the back of the crocodile. This procedure was done when the crocodile was treated with lignocaine anesthetic first. Later on, a radio telemetry tag transmitter were also attached to the tail area of the crocodile. The crocodiles were kept safely and were released when they regained conscious (Hamish et al., 2010 a).

Table 6 shows the results of Hamish et al., (2010 a), on the diving characteristics of the captured crocodiles. The crocodiles were categorized into 3 groups: the small size group 5-8kg, medium class 8-13kg and larger class 15-42kg. The table 6 shows that the smaller class crocodile shows the most total number of dives compared to the other 2 larger groups. This means that its active and resting dive were more than the 2 larger groups. The total number of resting dive was 4569 while active dive was 1800 for the smaller group crocodiles. Although smaller sized crocodiles showed the most number of dives for both active and resting dive, all 3 size classes showed similar resting dive resting dive to be more than the active dive number (Hamish et al., 2010 a). In terms of resting dive time, all 3 size class shows almost the same number or time spend during resting dive which was 11.5 to 12.9. This was also the same case for all 3 classes in active dive activity where the active dive was slightly in between 0.77-0.83. Both resting and active dive time for all 3 size classes of crocodiles increased slightly as the body size increased (Hamish et al., 2010 a). The only differences for all 3 size class of crocodiles, was that all 3 class resting dive time was always more than 1 minute time where as active dive for all 3 size groups was less than 1 minute time. For the amount of depth undergo by crocodiles for both active and resting dive, all 3 size classes shows a big difference in mean value. Smaller size classes shows a slightly deeper submerge depth 126.3 resting dive and 61.3 for active dive compare to medium class size crocodiles, but the deepest depth submerge was that of the largest size class which was 159.5 for resting dive and 75.5 for active dive. Crocodiles with larger body weight are able to dive at a greater depth regardless of active dive or resting dive because larger crocodile’s body structure enables them to withstand the high water pressure at the bottom when they submerge (Seebacher, 2001). Smaller sized crocodiles will have difficulties as they are not able to cope with strong water pressure at the bottom. This was not the case in table 6 as smaller crocodile dive slightly deeper than the medium classes including both active and resting dive because the smaller crocodiles are a potential prey for larger predator at the outside environment. Thus, they tend to dive a slightly deeper to prevent being spotted by predator. All 3 size classes show decrease in time for active and also resting dive (Hamish et al., 2010 a).

Figure 11 also from Hamish et al., ( 2010 a) results shows both different dive profiles of the captured Crocodylus johnstoni. A resting dive profile and also an active dive profile. The resting dive profile showed that the crocodile diving depth was constant in between 0-40 minute. They were no changes in depth during this period of time. After the 40 minute time, the profile seen was an active dive profile. From figure 11, crocodiles showed shifting depth during active dive. It was also clearly seen that active dive are not as deep as resting dive (Hamish et al., 2010a). The downwards arrows from the top indicates the lateral tail beats from the diving crocodiles. Only one lateral tail beat was seen at 0 minute time at the start of resting dive. After the 40 minute time, which was the end of resting dive but the start of active dive, the Crocodylus johnstoni showed greater lateral tail beat. The lateral tail beat during active dive was in great concentration and it happened most of the time (Hamish et al., 2010 a).

Hamish et al., (2010 a) showed that the maximum normal routine dive and the avoidance dive routine for the same Crocodylus johnstoni in figure 12. From the figure number, regardless of all different sizes, they all show that their maximum normal routine dive time length was around 100 minute. Only 1 crocodile with body mass over 40kg showed a maximum length of dive duration over 100 minute (Hamish et al., 2010 a). Compared to the avoidance routine, the crocodile length of dive time showed more around 200 minute time. And the maximum avoidance was shown by the over 40kg crocodile with a 400 minute time (Hamish et al., 2010 a).

Hamish et al., (2010 a), study results showed in figure 13, shows the number of lateral tail beats expressed per hour throughout diel cycle and also with which shows the mean hourly water temperature at 0.15m depth. Starting at 4 hour, the lateral tail beats produced were around 10 lateral tail beats per hour, when the surface water temperature was at 20 degree Celsius. (Hamish et al., 2010 a) The number of lateral tail beats per hour was seen rapidly increasing after the 15 hour and reached its maximum at the 20 hour as much as 40 lateral tail beats per hour when the water surface temperature was around 25 degree Celsius. The figure 13 also shows that when the surface water temperature rises the lateral tail beats of the crocodiles also increase (Hamish et al., 2010 a).

Figure 14 shows the result from Campbell et al, (2010a ) study. The total number of dive recorded during winter was 7472 much more compared to dives during summer time with 5955. The mean number of dive observed during winter was 38 percent greater then summer. This was similar to the median and also the maximum dive durations of the crocodiles that are shorter. Moreover, the proportion of each day that crocodiles were submerged also did not vary between seasons. During winter, most dives were less than 20 min duration but substantially greater proportion of time was spent on dives was more than 40 min. Figure 15 from Campbell et al, (2010a ) shows the mean body mass of observed crocodiles during both winter and summer season. There are no significant in the mean body mass between the 2 sample periods. The only thing which was different was the relationship of body mass and dive duration between both seasons. During summer time, the results show a positive nonlinear effect between dive duration and the crocodiles body mass. While during winter, it shows the opposite, body mass had little effect on dive duration (Campbell et al, 2010a ).

From the studies above by Hamish et al., (2010a), Campbell et al, (2010a ) and Elsworth et al., (2003) although absolute critical swimming speed (ms-1) increases as the body length of the crocodiles increases, the relative aerobic swimming performance (BLs-1) decrease as the crocodile body length increases. This problem can be explained by the hydrodynamic resistance theory. Hydrodynamic resistance stated that, the greater the surface area of the animal, it would therefore experience greater friction (Stelle et al., 2000). Looking at the body structure of crocodiles, its biomechanical design was a hybrid of a land and water animal features. It enables locomotion on land and also in water (Frey et al., 2001). When compared to fish, the water flow patterns and vortices surrounding the body will be far less than optimal (Drucker et al., 2000). The locomotion of crocodiles are also known to be affected by temperature as physiological mechanism such as metabolic rate and muscle activity are also depend on it, thus determine the whole animal performance (Elsworth et al., 2003). The temperature range of the metabolic plateau corresponds to that observed for the plateau in Ucrit of the crocodile which clearly indicate that maximal aerobic metabolic rates are limited sustained swimming performance. This shows that the metabolic rate of crocodiles increased continually over temperature ranges from 10-35 degree Celsius (Elsworth et al., 2003). Results shows that the limitation of aerobic dive duration was allometrically scale with body mass but external factors were also resulted in the allometric difference in dive behaviour. The amount of time where the crocodiles submerged elevated was associated with the daily minimum in lateral tail beat (LTB) activity. The high proportion of resting dive by the smaller crocodiles was because it needs some adjustment of the post-dive-surface-interval to clear an anaerobic debt (Costa et al., 2004). Crocodiles that are larger in body mass showed no correlation between dive duration and post dive surface interval suggesting that large majority of the resting dives were terminated before any significant lactate debt occurred. The depth of resting dives also showed a positive association with body mass. The relationship of body mass and the depth of resting dive suggest that the depth water act as a refuge for crocodiles. Evasion of predators will be the reason where crocodiles refuge during the early morning. Another reason was also because of low air and surface temperatures would have resulted in suboptimal muscle performance (Franklin et al., 2003). In some studies, such as Johnston et al., (2002), shows that the perfect compensation of swimming in low body temperatures of some crocodiles was because that their muscle function had already been remodelled to be optimized at a ‘new’ lower body temperature. Meaning that, its body had been modified chemically so that they are suitable to perform under lower body temperature. Long dive and with a resting phase enables them to conserve energy costs at the same time reducing risk of predation. After the day time period, air and surface temperature heat up and short shallower dives were seen gradually to increase and also aid with active dive. On the other hand, study of Campbell et al, (2010a ) on fresh water crocodiles, Crocodylus johnstoni, mean body temperature was higher during summer while the average dive duration significantly reduced compared to winter period. The relation of the dive duration with body mass during the summer period reduce in dive performance was due to the higher rate of oxygen consumption during dive activity. This was because that the crocodiles were all inactive during those extended dives and the diving metabolic rate must have been greater (Campbell et al., 2012). The results obtain from this study were similar to Jackson, (2007) studies of the effect of acute thermal exposure on diving air-breathing ectotherms. It also implies that inadequate thermal acclimatization of the diving metabolic rate occurred between both summer and winter (Jackson, 2007). Crocodiles from the results also show significant changes in the activities of regulatory metabolic enzyme after only a few weeks of thermal acclimatization (Glanville et al., 2006). In summer, the crocodiles showed less dives duration but more number of dives were done. The crocodiles during this period spend most of their time submerged. Study of Elsworth et al., (2003) and Hamish et al., (2010a) also shows that body mass relationship with dive duration was a poor indicator for crocodiles dive duration and ecological factors have a greater influence for diving activity compared to oxygen reserve (Campbell et al., 2010b). From the studies of Elsworth et al., (2003), Hamish et al., (2010a) and Campbell et al, (2010a ), the findings for crocodiles tested during summer, showed opposite results, where dive duration was affected by crocodiles body mass, but body mass of crocodile does not affect dive duration during winter. thus supporting the theory where crocodile’s oxygen reserves influences in controlling dive duration during summer and also winter period. The diving of crocodiles resulted during summer shows shorter duration lead to hypothesis, that diving metabolic rate was greater (Campbell et al., 2010b).

Figure 8: Effect of body length on critical swimming speed at 18 °C and 33 °C for Crocodylus porosus.

(Elsworth et al., 2003)

Figure 9: Effect of body length on length-specific critical swimming speed at 18 °C and 33 °C of Crocoylus porosus.

(Elsworth et al., 2003)

Figure 10: The effect of temperature on length-specific critical swimming speed for small, medium and large size classes of Crocodylus porosus.

(Elsworth et al., 2003)

Table 6: Diving characteristic of Crocoylus johnstoni grouped by body mass

(Hamish et al., 2010a)

Figure 11: Two different dive profiles for captured Crocodylus johnstoni. A resting-dive with extended bottom duration and no change in depth and an active-dive with a shifting depth. Down ward arrows indicate timing of lateral tail beats during dive type.

(Hamish et al., 2010 a)

Figure 12: The maximum normal routine dive duration (black circles) and avoidance dive routine (white circles) for the same Crocoylus johnstoni.

(Hamish et al., 2010 a)

Figure 13: The number of lateral tail beats expressed per hour throughout diel cycle (black circles) and the mean hourly water temperature at 0.15 m depth (white circles).

(Hamish et al., 2010 a)

Figure 14: Dive duration of G.johnstoni recorded in winter (white bars) and summer (black bars) as a proportion of the total time within each duration bin. Dive duration bins represent 0.8 min increments.

(Campbell et al, 2010a )

Figure 15: Relationship between dive duration of C.johnstoni with body mass. The influence of winter (grey line) and summer (black line).

(Campbell et al, 2010a )

3.0 General discussion

Crocodiles regardless of species showed ontogenic shift in prey choice (Agata, 2011). Fish are the primary main diet consumed by crocodiles. As their body size increases, their diet varies to a wider range which consists of mammals and birds. These are due to the consequences of jaw development. Adults females from Alejandro, (2008) show that it consumes almost 99 percent of crustacean’s diets which was due to reproduction period. Crocodiles need more calcium minerals for egg clutches production. Wallace et al., (2008) also proved that they consumed carrion. The effective digestion of crocodile’s diets occurs at only certain temperature range (Cherkiss, et al., 2011). They feed less during the hot day and that cooler temperature decrease the rate of digestion. As stated by Downs et al., (2008), crocodiles are similar to other reptiles where their body temperature easily increases rapidly but the cooling rate of body will be much slower. The basking period of crocodiles usually starts in between the 8 and 11 hour. Venugopal et al., (2003) stated that crocodiles basking will be delayed a little during an extreme hot day as they are seen to submerge more. Land basking of crocodiles happens when the surrounding was greater than the water temperature (Venugopal et al., 2003). During rainy days, Crocodiles tends to stay longer submerging and only out on shore at a later period to bask, usually later than 10.00 (Downs et al., 2008). The water acts as a heat source or a heat sink depends on the condition of the environment outside. Juvenile crocodiles are seen basking earlier then the sub adults and adult crocodiles. For the locomotion of crocodiles, the absolute critical swimming speed (ms-1) increased as the body length of crocodile increased. The relative aerobic swimming performance (BLs-1) decreased as the crocodile body length increased, which was the opposite to swimming speed (ms-1). This was because, hydrodynamic resistance stated that the greater the surface area of the animal, the greater the friction force it will experience (Stelle et al, 2000). The swimming and diving of crocodile were also known to be effected by temperature as metabolic rate mechanism and muscle activity are dependent on it (Elsworth et al., 2003). The study by Elsworth et al., (2003), showed that the metabolic rate of crocodiles increase continues over temperatures ranges from 10-35 degree Celsius. The total time where crocodiles submerged increases was associated with daily minimum in lateral tail beat (LTB) activity. Moreover, the high percentage of resting dive shown by juvenile crocodiles was because they needed adjustment for post dive surface interval to clear an anaerobic debt (Costa et al., 2004). Evasion of predators usually by juvenile’s crocodiles was the reason why crocodiles refuge in morning. Another reason to support the sentence was that the muscle performance was below optimal due to the low air and surface temperatures (Elsworth et al., 2003). Jackson, (2007) also impels the thermal acclimatization of the diving metabolic rate occurred between both summer and winter. During summer time, fewer active dives were seen, while resting dive were more. All crocodiles during this period spend their time submerged (Seebacher, 2000).

4.0 Conclusion

Crocodiles shows ontogenic shift in prey choice. They are opportunistic feeders that feed on a wide range of diets. Their diets range from small land invertebrates, small fish, crustaceans, larger fish and finally larger animals such as mammals and birds. Their range of food varies as they get larger from juvenile to adult crocodiles. This was because that their jaws morphology gets wider and stronger. Crocodiles are cold blooded and their body metabolism was slow. Thus, they thermoregulate to maintain their body temperature at optimum level so that they can carry out their daily performances. The basking activity of crocodiles varies among season and was highly dependable on the outside condition and environment. When basking, they prefer to bask on land, but basking on water surface or in between 2 medium was also possible, depending on the condition and environment. In terms of locomotion, crocodiles swimming and diving activity are also dependent on the surrounding temperature. Moreover, their swimming and diving performances are also greatly affected by their body size and length. This was because of the hydrodynamic resistance theory, where larger surface area animals tend to have the greatest fiction force. This theory explains that, although the swimming speed of adults crocodiles are greater, they can easily get fatigue and can not last long when compared to juvenile crocodiles. Diving of crocodiles was divided into 2 which was the active dive and the resting dive. Resting dive, was not much movement seen from the crocodiles and is usually submerge, while active dive are associated with swimming and hunting performance. Finally, the diving of crocodiles were seen longer when they are in threat. This type of dive was known as avoidance dive, where the diving duration is slightly longer than normal dive.