Population Size and Structure of the Nile Crocodile Crocodylus Niloticus in the Lower Zambezi Valley

Population size and structure of the Nile crocodile Crocodylus niloticus in the lower Zambezi valley

K EVIN M. WALLACE,ALISON J. LESLIE,TIM C OULSON and A UDREY S. WALLACE

Abstract Concern has been raised about the lack of resilience to harvesting (Velasco et al., 2003). Habitat population data for the Nile crocodile Crocodylus niloticus loss (Thorbjarnarson et al., 2002) and human–crocodile in the lower/middle Zambezi valley. This area is important conflict (McGregor, 2005) are also exerting pressure on for conservation as well as being a source of crocodile eggs crocodilians. The multitude of threats is a serious concern and adults for the ranching industry. Two spotlight surveys, and monitoring of populations is a critical process in the in 2006 and 2009, were used to estimate population size, management of any species. Despite this, of the many structure and trends. A stage-structured matrix model was surveys of crocodilians throughout Africa only a small parameterized from existing literature and the expected percentage facilitate estimation of population trends predictions were compared to those observed. The survey because of temporal, spatial and methodological incon- data suggests a population increase since 2006. Crocodile sistencies (Lainez, 2008), and therefore the status of −1 density was greatest (3.1 km ) in the areas of increased crocodiles in Africa is not well-known. −1 wildlife and habitat protection and lowest (1.4 km ) in areas The Nile crocodile Crocodylus niloticus in Zambia and of increased human presence. The predicted population Zimbabwe is categorized as Lower Risk/least concern on the stage structure differed to that observed, suggestive of a IUCN Red List (Crocodile Specialist Group, 1996). It is listed population not at equilibrium. Data on offtakes of crocodile on Appendix II of CITES, which denotes a species not eggs and adults would be useful for examining why this is necessarily threatened with extinction but one that may the case. Continued monitoring of the wild population is become so unless trade is closely controlled. The wild necessary, to evaluate the trend of an increasing crocodile crocodile population in Zambia and Zimbabwe remains an population, and additional demographic data for modelling important resource for the crocodile farming and ranching purposes would be desirable. industry through the harvesting of eggs and adult breeding stock. It has been noted that continuation of this practice Keywords Conservation, Crocodylus niloticus, manage- alongside a lack of baseline scientific data may have ment, matrix model, Nile crocodile, spotlight survey, a detrimental effect on the wild population (Siamudaala Zambezi valley et al., 2004). This paper contains supplementary material that can be If the size and structure of the wild population can be found online at http://journals.cambridge.org estimated, this information can be used to compare the results with a theoretical model, as this can provide insight into whether the study population is typical of other populations of the same species. Such insight can help Introduction inform management plans. Population models have been developed for numerous crocodilian species (Smith & fi rocodilians ful l an essential ecosystem role (Mazzotti Webb, 1985; Craig et al., 1992; Tucker, 2001; Gallegos et al., 2009 Cet al., ) and have inherent commercial value for 2008). One of the simplest models used to predict growth 2002 both the leather industry (Hutton et al., ) and tourism rates and stable stage structure is a discrete stage-structured 2008 (Telleria et al., ). Overexploitation can cause population model (Caswell, 2001), which facilitates predictions of crashes, leaving some populations potentially vulnerable the growth rate, stage structure, reproductive input and 2009 (Bishop et al., ) or critically threatened (Ballouard sensitivity analysis (Caswell, 2001). This demographic 2010 ff et al., ). Conservation e orts have allowed some analysis can offer valuable information for the management 2000 populations to recover (Webb et al., ). Sustainable util- of species. The models are used to simulate the impact of ization of crocodilians is possible and some species show intervention scenarios, such as the effect of harvesting animals of a certain size or increasing the survival of

KEVIN M. WALLACE (Corresponding author) TIM COULSON and AUDREY individuals. Analyses conclude that perturbations to the S. WALLACE Imperial College London, Division of Ecology and Evolution, survival of the mature breeding size class (e.g. by trophy Silwood Park, Ascot, Berkshire, SL5 7PY, UK. ﬀ E-mail [email protected] hunting) have a greater e ect on population growth than that of perturbations at the egg stage or smaller size classes ALISON J. LESLIE Department of Conservation Ecology and Entomology, Faculty 1992 2001 of Agrisciences, University of Stellenbosch, South Africa (Craig et al., ; Tucker, ). This is useful as ﬁ Received 16 June 2011. Revision requested 17 November 2011. conservation funds are often limited and speci cally Accepted 24 November 2011. targeting such funds at a part of the life cycle that results

© 2013 Fauna & Flora International, Oryx, 47(3), 457–465 doi:10.1017/S0030605311001712 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 29 Sep 2021 at 09:01:58, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605311001712 458 K. M. Wallace et al.

in the desired outcome in the most cost-effective way is surveyed up to 20 km from the confluence, where shallow important. rapids prevented further upstream travel. Nocturnal spotlight surveys are the most commonly There are four levels of wildlife/habitat protection: used technique for evaluating crocodile populations and open areas, game management areas, safari areas and trends over time. Difficulties encountered during such protected areas. Open areas allow human settlement, surveys can range from physical access to areas, and technical development and agriculture. Game management areas bias such as observer skill and boat speed (Cherkiss et al., allow settlement and agriculture but also act as a buffer zone 2006), to environmental variables such as water level for protected areas. Safari areas do not allow human and temperature (Hutton & Woolhouse, 1989). The settlement or agriculture but permit wildlife hunting and technique can underestimate populations because of these harvesting quotas (as do open areas and game management difficulties and because of the cryptic nature of crocodiles areas). The two protected areas (Lower Zambezi National (Bayliss et al., 1986; Hutton & Woolhouse, 1989). Therefore Park and Mana Pools National Park) have the highest the results of spotlight surveys are often interpreted as levels of wildlife/habitat protection and are no-take zones a population index. The real population size is often for wildlife. The human population is highest along the unknown as complete counts of an entire study site are Zambian riverbank, being most concentrated in the Chiawa rarely possible. Population indices are estimated from Game Management Area and the Siavunga Open Area, incomplete counts that may incorporate correction factors although there are numerous tourist and hunting lodges (Hutton & Woolhouse, 1989; Fergusson, 2006). Repeated along the entire length of the Zambezi River in both Zambia standardized spotlight surveys are the most common form and Zimbabwe. To maintain consistency with the 2006 of population monitoring for crocodiles (Seijas & Chavez, survey the study site was separated into two main sections, 2000). As long as a bias is consistent, the population the eastern section, Kanyemba to Ruckomechi (the upstream index will remain relative to the true population count border of Mana Pools), which includes the National Parks, and inferences can be made from the population index and the western section, Ruckomechi to Nyamumba, which in subsequent years of surveys to establish population has a lower overall level of wildlife/habitat protection and trends. The estimates should be interpreted carefully but are a higher level of human population and agricultural still the primary indicator of population status for development. crocodilians. This study is a follow-up survey to that of Fergusson Methods (2006). Our objectives were to (1) compare our 2009 spotlight survey with that of 2006,(2) parameterize a stage- Research protocols were similar to that of Fergusson’s structured matrix model for C. niloticus, and (3) compare (2006) survey, to facilitate comparisons. A nocturnal the predicted population structure from the model to that spotlight survey was used to census the population from a observed in the wild. We discuss the results in terms of 5-m swamp cruiser boat powered by a 60-hp outboard motor management recommendations. during September, the same month as the 2006 spotlight survey. The survey was timed to coincide with the new Study area moon phase (the darkest period of the month). The weather was cloudless with calm river conditions, good visibility The stretch of the Zambezi River between Kariba dam and the mean air temperature (27.3 ± SE 0.1°C) exceeded and Cahora Bassa has been termed both the lower and that of the temperature (24.7 ± SE 0.1°C), providing optimal middle Zambezi, hereafter we refer to this area as the lower spotlighting conditions (Hutton & Woolhouse, 1989). The Zambezi. The area has a distinct wet season during water level was low prior to the wet season (November– November–April, followed by a cool dry season (May– April), when the water level peaks. The same experienced July) and a hot dry season (August–October). The lower spotlighter and coxswain were used for each night shift Zambezi study area (Fig. 1) extends from Nyamumba at the during the survey. western extreme to the confluence of the Zambezi/Luangwa Only one survey boat and crew were available and River (Kanyemba) in the east and is c. 270 km long, therefore only one bank could be surveyed at a time because following the main Zambezi channel. The lower Zambezi of the width of the river (c. 500 m). The Zimbabwe riverbank River is relatively shallow and wide with occasional islands was surveyed first (4 days), then the Zambia riverbank and it meanders between floodplains on either side. The (5 days; the additional day being used to survey the lower River is navigable although sandbars can restrict travel by reaches of the Kafue River). Each local region of the study boat in certain areas. The Kafue and Luangwa Rivers are the site constituted a consecutive night survey. The main bank only two major tributaries that enter the Zambezi. Because was followed at a distance of 5–10 m from the shoreline and, of its size and lack of navigability the Luangwa River was where possible, islands were circumnavigated. Crocodiles not surveyed. The lower reaches of the Kafue River were were located by eye-shine using a 500,000 candle-power

© 2013 Fauna & Flora International, Oryx, 47(3), 457–465 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 29 Sep 2021 at 09:01:58, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605311001712 Nile crocodile in the Zambezi valley 459

15°0'S

15°30'S

16°0'S

16°30'S

FIG. 1 The lower Zambezi study site, with the main rivers (Zambezi, Kafue and Luangwa). The Zambezi River forms the international border between Zambia and 17°0'S Zimbabwe. OA, Open Area; GMA, Game 28°30'E 29°0'E 29°30'E 30°0'E 30°30'E Management Area; SA, Safari Area.

spotlight. The survey was undertaken travelling upstream are hereafter referred to as the ‘capture surveys’. Crocodiles −1 (8–12 km h ); the spotlight beam was traversed through an that were seen but not caught were recorded, with a size arc of 180° illuminating the riverbank and main channel. estimate when possible. These data are used to validate our The upstream direction was chosen for safety reasons and 2009 spotlight survey by providing repeated surveys of boat control. When eye-shine was observed, the crocodile the same sections of river, and to estimate the sex ratio was approached as closely as possible to estimate its total of the population from captured animals. length. If the entire animal could not be seen estimation of total length was based on the head length, exposed above the Analysis water line. This allowed extrapolation to total length (7 × the 1987 length of the head; Hutton, ); this relationship was Google Earth v. 5.2.1 (Googleplex, California, USA) and ﬁ con rmed by morphometric measurements that we made ArcGIS v. 9.3.1 (ESRI, Redlands, USA) were used for 7 1 ± 0 11 5550 during a capture survey (mean . SE . ,n ). When mapping and measurement of the riverbank frontage. a crocodile submerged before the observer could estimate This included the main riverbanks of Zambia and the size, the sighting was recorded as eyes-only. A global Zimbabwe as well as the perimeter of all islands. Statistical positioning system (GPS) was used to map locations and analyses were performed using Rv.2.10.1 (R Development routes. Crocodiles were separated into four size classes Core Team, 2008). Linear regression was used to investigate ’ 2006 following Fergusson s( ) study: hatchlings and yearlings correlation between levels of protection/habitation and ,0 5 0 5–1 0 (total length . m); juveniles (total length . . m); crocodile density. The areas were assigned values 0, 1, 2 or 3, 1 0–2 5 subadults (total length . . m); adults (total length representing no, low, medium and high wildlife/habitat .2 5 . m). protection (corresponding to high levels of human habitation through to no permanent human habitation). The 0 1 Repeated area surveys values for each area were: , Siavunga Open Area; , Kafue River; 2, Chiawa and Rufunsa Game Management Areas; Between September 2007 and November 2009 other spot- 3, Hurungwe, Sapi and Chewore Safari Areas, Lower light counts were conducted as part of a capture study Zambezi National Park and Mana Pools. The values were using the spotlight technique described above and accepted used as explanatory variables for crocodile density per km. crocodile capture methods (Webb & Messel, 1977). These As spotlight surveys are renowned for underestimating

populations linear regression was used to investigate females in the population (0.54); EPC, mean eggs per clutch correlations between the maximum number of crocodile (45.48); NE, nest effort or proportion of reproductively sightings in the sections (using 6–20 repeated surveys) and active females that breed and nest (0.66); PR, proportion of the number of crocodiles seen during the 2009 spotlight eggs depredated (0.45); and φ, survivorship of adults (0.98). survey for that same section. As the spotlight data consisted The minimum size of a female breeding Nile crocodile is of count data, comparisons of crocodile population c. 2.3 m total length at c. 15 years of age, which falls within structure between areas, surveys and the matrix model the later part of the subadult stage. To maintain consistency were made using contingency tables. with the 2006 survey the subadult reproductive rate (F3)was calculated as the proportion of time reproductively active (total length 2.3–2.5 m, the last 4 years of the subadult class) Matrix model parameterization as a function of F4. Growth rates were derived by combining growth data across male and female C. niloticus (Hutton, The Nile crocodile life cycle was separated into four 1984; Games, 1990) and survivorship values estimated from ’ ontogenetic categories (following those of Fergusson s a study by Bourquin (2007). Sensitivities and elasticities 2006 survey in ) to estimate stage class for the matrix were calculated, as was the stable age distribution and 1 fi model. Stage represents the rst year, when hatchlings population growth rate (λ). enter a phase of high predation (hatchlings and yearlings, see above). Stage 2 represents the immature juvenile stage Results (juveniles) lasting 2 years, when the animals enter a period of reduced predation. Stage 3 represents the immature Spotlight survey to early mature subadult stage (subadults) lasting 19 years. 4 Stage represents the adult age class (adults), when A total of 1,761 crocodiles were encountered during the individuals enter the main reproductive portion of the spotlight survey in 2009, a third (33.8%, n5595) were 28 population, lasting c. years, completing the presumed classed as eyes-only sightings. The size class structure was 50 2 -year life cycle in the wild. The survivorship values are skewed towards the smaller size classes (χ 5194.7,P, 0.01, distributed between the potential of an animal surviving df 52), 51.5% were juveniles (n5 601), 29.7% subadult and moving from one stage to the next (Gi) or surviving and (n 5346) and 18.8% adult. During the capture surveys a remaining in the same stage (Pi). Here we use the duration total of 505 individual crocodiles were caught; n579 (15.7%) fi of each stage (dj) and overall stage-speci c survivorship (Pi) yearlings; n5311 (61.6%) juveniles; n5112 (22.2%) sub- 2001 following methods of Caswell ( ): adults; n54 (0.6%) adults. The overall sex ratio of captured The transition matrix for the stage classification is: 52 8 47 2   individuals was . % male to . % female. There was a 00F3 F4 strong correlation between the number of crocodiles sighted  G1 P20 0 during the spotlight survey and the maximum number A =    0 G2 P30 sighted for that particular section during the repeated area 2 00G3 P4 surveys (r 50.93 P, 0.01,df5 6). Overall the spotlight survey recorded 0.84 ± SE 0.05 of the maximum number of Pidj(1 − Pi) crocodiles seen in the same areas as determined by the Gi = 1 − Pidj capture surveys. Assuming random and non-selective spotting and 1 − Pidj−1 Pi = Pi catching, both surveys (spotlight and capture) would be 1 − Pidj expected to show similarities in the percentages of size classes seen. However, there were differences between the =( )( )( )( )(φ) F4 PF EPC NE PR overall percentages of the size classes identified in the 2 spotlight survey and the capture surveys (χ 5235.3, F3 =(duration subadult is reproductive/ P, 0.01,df53). The spotlight survey recorded more adults ) total years subadult F4 (12.4%) than the capture surveys (7.7%) and fewer subadults   (19.6 and 30.1%, respectively). The two surveys recorded . . 001572 similar juvenile (34.1 and 31.1%, respectively) and eyes-only  0.12 0.32 0 0  A =   sightings (33.8 and 31.2%, respectively).  00.15 0.94 0  The crocodiles were not equally distributed throughout 000.04 0.95 the study site, with considerable variation in encounter rates Demographic parameters for the matrix were obtained for the different areas (Table 1). Crocodile density increased in 2 from existing literature (Supplementary Table S1). Adult areas with higher protection (r 50.79,P50.01,df57), from −1 −1 reproductive rate (F4) depended on PF, the proportion of Siavunga Open Area (0.9km ) to Mana Pools (5.4km ).

TABLE 1 Demographics of Nile crocodile Crocodylus niloticus in the lower Zambezi valley (Fig. 1), estimated from a spotlight survey in 2009. Protection is an estimate of wildlife/habitat protection (see text for details). Riverbank is the main shoreline and does not include islands because of the diﬃculty in determining if they are Zambian or Zimbabwean.

% % % % No. of River bank Crocodile − Region (by country) Protection juveniles subadults adults eyes-only crocodiles seen length (km) density (km 1) Zambia Siavunga Open Area None 54.7 15.1 5.7 24.5 53 56 0.9 Chiawa Game Management Moderate 56.8 14.2 8.0 21.0 162 58 2.8 Area Lower Zambezi National Park High 32.8 9.6 25.5 32.2 491 107 4.6 Rufunsa Game Management Moderate 66.7 8.3 8.3 16.7 36 30 1.2 Area Kafue River Low 61.0 16.9 8.5 13.6 59 40 1.5 Zimbabwe Hurungwe Safari Area High 40.3 15.1 9.7 34.9 186 80 2.4 Mana Pools High 12.2 12.5 27.5 47.9 353 66 5.4 Sapi Safari Area High 46.8 8.2 5.7 39.2 158 33 4.8 Chewore Safari Area High 44.5 20.9 4.2 30.4 263 74 3.6 Total 13.1 16.1 33.8 37.0 1,761 544 3.2

TABLE 2 Percentage of C. niloticus size classes (including unclassiﬁed eyes-only sightings) in the lower Zambezi River in 2006 (from 2 Fergusson, 2006) and 2009. The size structure of the sections is compared using χ contingency tables. The western section is the area between Ruckomechi and Nyamumba (263 km of riverbank); the eastern section is from Kanyemba to Ruckomechi (504 km of riverbank).

Size category (%) No. of Year Section Juveniles Subadults Adults Eyes-only crocodiles seen χ2 df P 2006 Western 47.6 8.1 2.8 41.5 246 15.7 3 ,0.01 Eastern 22.8 8.5 16.7 52.0 1,124 2009 Western 38.2 22.3 6.6 32.9 319 77.3 3 ,0.01 Eastern 32.3 18.9 14.0 34.9 1,383

The population structure of the two main river sections boat between sightings. For the purpose of comparison the differed in both the 2006 and the 2009 surveys (Table 2). 2006 population estimate was corrected with the 2009 The overall percentage of crocodiles sighted (including eyes- riverbank measurements. There was an overall increase −1 −1 only) in the eastern section in 2006 and 2009 were similar in density from 2.2 km in 2006 to 2.5 km in 2009. −1 (81.3 and 81.5%, respectively), and also in the western section The eastern section had a slight increase from 3.0 to 3.1 km −1 (18.7 and 18.5%, respectively). The 2009 measurements of and the western section 0.6 to 1.4 km . The final corrected riverbank indicate that the eastern section was twice population estimate (Table 3)in2009 was c. 2,257 crocodiles, the length (67%) of the western section (33%). The The 2006 estimate was c. 1,984. Over the 3 years there was a approachability of crocodiles did not differ greatly between larger increase in the number of crocodiles in the western the eastern and western areas during 2006 (eyes-only (29.7%) than in the eastern section (23.0%). sightings 50.4 and 41.3% respectively) and 2009 (34.9 and 32 9 . %). Matrix model Crocodile density differed between the 2006 and 2009 surveys because of a disparity in bank length measurements The population size structure of the crocodiles recorded in for the same sections. The eastern section was measured as both the 2006 and 2009 surveys differed from that predicted 268.9 km in 2006 and 599.0 km in 2009, the western section by the matrix model. A much lower percentage of juveniles as 207.5 and 295.0 km respectively. This is a large disparity and a higher percentage of subadults were estimated by the and we are confident that the 2009 measurements are matrix than was seen on either spotlight survey throughout accurate. It is doubtful that bank erosion would have caused the entire study site or in the western and eastern sections such a change. The 2009 measurements follow the contours separately (Fig. 2). To achieve the observed population of the banks on either side of the River. We surmise, structure it was necessary to perturb the matrix parameters therefore, that the 2006 measurements are of the route of the to a substantial (and unrealistic) extent by reducing subadult

TABLE 3 Population estimates of C. niloticus on the lower Zambezi 100 River based on a spotlight survey. Riverbank is the actual shoreline Juvenile of the mainland and islands. Unsurveyed riverbank (km) is the Subadult 80 distance not covered by the survey because of inaccessibility. This Adult was derived by comparing the GPS route to an image of the study 60 area, in ArcGIS. Correction for riverbank is the percentage of

riverbank omitted during the survey. Correction for survey was Percentage 40 estimated using data of repeated surveys of the same sections.

Western Eastern 20 section section Overall 0 Riverbank (km) 263 504 767 2006 2009 2006 2009 2006 2009 Western section Eastern section Overall Matrix Absolute numbers seen 319 1,383 1,702 Sightings classified 67.1% 65.1% 65.5% FIG. 2 Size structure of Crocodylus niloticus determined from spotlight survey counts during September 2006 (Fergusson 2006) Unsurveyed riverbank (km) 32 95 127 2009 Correction for riverbank +12.2% +18.8% +16.6% and (this survey), overall (western and eastern sections Correction for survey +16.0% +16.0% +16.0% combined) and from a stage-based matrix model. Corrected total no. of crocodiles 409 1,864 2,257 −1 Corrected crocodiles km 3.7 1.2 2.2 two boats (one for each bank) would have been ideal but logistical problems precluded this. We assume there is no bias because of crocodiles crossing the river between Zambia 0 60 λ50 97 survivorship to . ( . ). Increasing juvenile survival and Zimbabwe as each crossing could be countered by to represent a higher percentage of that stage class in turn another in the opposite direction. increased the larger size classes. The unperturbed matrix The same densities of crocodiles were sighted in the 5 predicted a population growth rate of c. % per year, which two sections of the Zambezi in both spotlight surveys. is feasible given the observed population growth rate Crocodile density was highest in the eastern section, which 2006 2009 between the and spotlight survey estimates. is characterized by increased wildlife/habitat protection. The reproductive values increased with body size: yearling This demonstrates the positive influence of protected 0 8 6 9 33 3 59 0 . %, juvenile . %, subadult . % and adult . %. The areas for conservation of this crocodile. However, the rate 66 9 11 1 predicted stable stage structure was . % yearling, . % of population increase was lower in the eastern section 15 6 6 5 juvenile, . % subadult and . % adult. When the yearling than the western section. There is a possibility of density- 33 4 percentage is omitted the stage structure became . % dependent factors controlling population growth, which has 47 1 19 5 juvenile, . % subadult and . % adult. The elements in been described in other studies (Velasco et al., 2003). 4 the sensitivity matrix (Table ) indicate that growth from A deterministic matrix predicts that a population the subadult to the adult stage has the highest sensitivity converges to a stable stage distribution. In the wild po- 0 89 0 45 ( . ), with subadult persistence ( . ) and probability of pulations are not deterministic but a population fluctuating 0 34 0 34 growing ( . ) and remaining an adult ( . ) exhibiting the around equilibrium may nevertheless have a structure highest elasticities. Expected number of replacements was close to that predicted by a deterministic model. The large 3 2 . per individual and the mean age of a reproductively disparity between prediction and observation suggests 35 0 active female was . years. either a problem with the model, a population a long way from equilibrium, or bias in the data (such as with the eyes- Discussion only data). The latter constitutes a substantial proportion of the sightings yet cannot be included within the size The lower Zambezi crocodile population size reported here classifications unless further assumptions are made; e.g. is a minimum estimate. Spotlight surveys tend to under- that they are all adult crocodiles. estimate actual densities (Hutton & Woolhouse, 1989). The The size class structure in the eastern section was similar use of correction factors is an attempt to estimate the actual in 2006 and 2009. The largest disparities are in the western population size given the biases involved with the survey section. The large proportion of eyes-only sightings in both technique. Nonetheless it appears that the lower Zambezi surveys makes it difficult to draw accurate conclusions, crocodile population increased between 2006 and 2009. however. The size and therefore the size class allocations The observed and predicted λ are close yet the observed of a third of sightings were not obtained and so it is difficult population structure differs from that expected in the to categorize these animals. It is possible that these are matrix model given the demographic rates published in the larger, more wary animals. Previous studies have the literature (Craig et al., 1992; Tucker, 2001). indicated that recapture probabilities decrease with in- Despite the biases of spotlight surveys our results provide creasing crocodile size (Bourquin, 2007) because of human a useful estimate of the crocodile population. A survey with disturbance, including from capture and release techniques

TABLE 4 Sensitivity and elasticity values for C. niloticus matrix elements. The matrix notation indicates values for an animal surviving and remaining in the same stage (Gi); surviving and moving from one stage to the next (Pi); and reproductive rate (Fi) for yearling (1), juvenile (2), subadult (3) and adult (4) size classes.

Matrix Sensitivity Elasticity 123412341234 1 F3 F4 0.01 0.00 0.02 0.03 2 G1 P2 0.45 0.07 0.05 0.02 3 G2 P3 0.36 0.50 0.05 0.45 4 G3 P4 0.89 0.37 0.03 0.34

(Ron et al., 1998). The western section is the most exploited The population thus appears to be drifting towards the part of the lower Zambezi study site for crocodile ranching theoretical stable stage structure. When comparing the and hunting (regulated by the wildlife departments of western and eastern sections the difference in relation to Zambia and Zimbabwe). Although exploitation does occur the matrix prediction is apparent. The eastern section is in the Zambia Rufunsa Game Management Area as well more similar to the prediction than the western, which is as the Zimbabwe safari areas, the overall level of protection characterized by a large proportion of smaller crocodiles. for the eastern section is higher. Crocodile ranching quotas This could be explained by an offtake of larger individuals, usually stipulate the number of eggs and breeding adults skewing the size structure towards the smaller size classes. (mainly females), and trophy hunting includes the larger It is not known if this population has suffered a major animals. Data on the actual offtake and locations are perturbation in the past. However, the area is subject to unavailable but would shed light on the difference between harvesting of crocodile eggs and adults, sanctioned by the the population age classes. The observed disparities could Zambian Wildlife Authority, and it is therefore difficult also be because of other forms of disturbance to the to estimate how many years the population would require population, including habitat issues. The Chiawa Game to reach an equilibrium given the population structure in Management Area (part of the western section) has an 2006. increasing human population and agricultural activities. A high sensitivity value indicates that an independent This could reduce available basking and nesting areas and change in that matrix element could cause a considerable increase harassment by humans. change in the expected population growth rate. This was The lower Zambezi includes areas allocated for crocodile found to occur in the transition phase from subadult to ranchers to collect live adults. The western section has adult at c. 2.5 m total length (c. 22 years). This size of animal the greatest proportion of this harvesting, which uses the would be desirable for crocodile farming: small enough same spotlight technique as our research team. It could to capture, at reproductive prime and with enough expected be surmised that the crocodiles in the western area were remaining life expectancy to adjust to captivity. This subject to a higher effort of capture for harvest or research. suggests that the targeted animals are within the class that However, this did not appear to affect the wariness of has the greatest potential to affect the population. Elasticity crocodiles as the ratio of sightings to eyes-only (possibly predicts the proportional change in the growth rate given a more wary crocodiles) were similar for the western and proportional change in the matrix element, while all other eastern sections. Although eyes-only sightings were elements remain constant. The highest elasticity values are highest in the eastern area this may have been because of remaining in the subadult and adult stage. This finding physical limitations rather than crocodile wariness. Navi- concurs with models that predict that the harvesting of gation in the eastern section was more difficult (especially larger individuals, especially those at sexual maturity, will in the Lower Zambezi National Park and Mana Pools) have a disproportionately large effect on the rate of change because of shallows, sand bars, submerged obstacles and of the population (Enneson & Litzgus, 2008). The sensitivity a higher density of potentially dangerous animals such as and elasticity values are lowest for the fecundity rate and the hippopotamus Hippopotamus amphibius. the earlier life history stages. This concurs with current If we assume that the size structure estimates are accurate management strategies that removal of eggs and hatchlings and that the population is not subject to duress then the from the wild will have the least effect on the growth rate observations would show a trend towards the stable stage of the wild population. Elasticity values are useful for structure predicted by the matrix. This would require a formulation of conservation plans but need to be inter- reduction in the number of individuals in the juvenile preted with considerable care (Mills et al., 1999) because size class, increase in the subadult class and reduction in they assume the effects of perturbing a demographic rate is the adult class. This pattern can be seen in a comparison linear, and the model assumes no density dependence or of the results of the 2006 survey with our 2009 survey. environmental stochasticity. Typically, matrix elements

with high elasticity values are targeted by management Zambezi who assisted the project (Zambezi Breezers plans as a high priority, with less emphasis placed on those Lodge, Kanyemba Lodge, Chongwe River Camp, Sausage elements that have low rates. In density-dependent models Tree Camp, Kulefu Camp, Mwambashi River Lodge, Anna a perturbation to one element will in turn affect all other Tree Lodge, and Andrew and Julie Woodley of Fringila), and matrix elements. Results of perturbations in the natural Davie and Ardri Visser at Baya Baya farm. Financial support system can differ substantially from predictions. In addition, was provided by the Earthwatch Institute and the National certain age/stage classes may be more or less susceptible to Environment Research Council, UK. conservation measures and may react unpredictably. The matrix represents a deterministic theoretical population References and in the natural environment there are many factors that fl can in uence the population but have not been included BALLOUARD, J.M., PRIOL, P., OISON, J., CILIBERTI,A.&CADI,A. in this simulation. Factors such as temperature-dependent (2010) Does reintroduction stabilize the population of the critically sex determination, density dependence, prey abundance endangered gharial (Gavialis gangeticus, Gavialidae) in Chitwan and nest site availability could all influence population National Park, Nepal? Aquatic Conservation: Marine and Freshwater Ecosystems, 20, 756–761. demography. Despite this, the matrix does offer an BAYLISS, P., WEBB, G.J.W., WHITEHEAD, P.J., DEMPSEY,K.& opportunity to examine whether the Zambezi population SMITH,A.(1986) Estimating the abundance of saltwater crocodiles, conforms to our general understanding of crocodilian life Crocodylus porosus Schneider, in tidal wetlands of the Northern histories. Territory—a mark-recapture experiment to correct spotlight counts Our results indicate an increasing crocodile population to absolute numbers, and the calibration of helicopter and spotlight counts. Australian Wildlife Research, 13, 309–320. that is still far from equilibrium. Future surveys are required BISHOP, J.M., LESLIE, A.J., BOURQUIN, S.L. & O’RYAN,C.(2009) to validate this trend. The importance of protected areas is Reduced effective population size in an overexploited population clearly illustrated yet there is evidence that the population of the Nile crocodile (Crocodylus niloticus). Biological Conservation, is increasing at a faster rate in areas that have a lower density 142, 2335–2341. of crocodiles. It is important to monitor the patterns of BOURQUIN, S.L. (2007) The population ecology of the Nile crocodile land-use change, especially in the game management and (Crocodylus niloticus) in the Panhandle region of the Okavango Delta, Botswana. PhD thesis. University of Stellenbosch, open areas, as loss of habitat has been cited as one of Stellenbosch, South Africa. the main causes of crocodile population decline. Additional CASWELL,H.(2001) Matrix Population Models: Construction, information regarding the harvesting and hunting of Analysis, and Interpretation. Sinauer Associates, Sunderland, USA. animals is required, as identifying this offtake (specimen CHERKISS, M.S., MAZZOTTI, F.J. & RICE, K.G. (2006)Effects size as well as numbers) will assist with the monitoring and of shoreline vegetation on visibility of American crocodiles fi (Crocodylus acutus) during spotlight surveys. Herpetological Review, management of the population. Our ndings will be passed 37, 37–40. to the appropriate authorities (government and NGOs) that CRAIG, G.C., GIBSON, D.S.C. & HUTTON, J.M. (1992) A population are involved with the management of crocodiles in Zambia model from the Nile crocodile and simulation of different and Zimbabwe. There has been no active crocodile research harvesting. In The CITES Nile Crocodile Project (eds J.M. Hutton 2009 & I. Games), pp. 1–52. CITES Secretariat, Lausanne, Switzerland. in this area since but we recommend repeating the 1996 3 CROCODILE SPECIALIST GROUP ( ) Crocodylus niloticus.InIUCN survey at intervals of years, to maintain population Red List of Threatened Species v. 2012.1. Http://www.iucnredlist.org monitoring. Any future project could usefully involve the [accessed 27 September 2012]. local crocodile farming industry as they also have an interest DETOEUF-BOULADE, A.S. (2006) Reproductive Cycle and Sexual Size in maintaining a viable crocodile population. Dimorphism of the Nile Crocodile (Crocodylus niloticus) in the Okavango Delta, Botswana. MSc thesis. University of Stellenbosch, Stellenbosch, South Africa. Acknowledgements ENNESON, J.J. & LITZGUS, J.D. (2008) Using long-term data and a stage-classified matrix to assess conservation strategies for an We wish to acknowledge the Zambian Wildlife Authority endangered turtle (Clemmys guttata). Biological Conservation, (ZAWA) and Zimbabwe Parks and Wildlife Management 141, 1560–1568. Authority (ZPWMA) for their assistance. Research permits FERGUSSON,R.(2006) Populations of Nile crocodile (Crocodylus were obtained from ZAWA and ZPWMA and the study niloticus) and hippopotamus (Hippopotamus amphibius) in the Zambezi. African Wildlife Foundation, Zambezi Heartland. complied with all appropriate ethics, guidelines and GALLEGOS, A., PLUMMER, T., UMINSKY, D., VEGA, C., WICKMAN,C. regulations. The research protocols were approved by the &ZAWOISKI,M.(2008) A mathematical model of a crocodilian Ethical Review Process of Imperial College London, UK. population using delay-differential equations. Journal of We thank Kerri Radmeyer, Adrian Hudson and the staff at Mathematical Biology, 57, 737–754. 1990 Conservation Lower Zambezi for logistical assistance, Pete, GAMES,I.( ) The feeding ecology of two Nile crocodile populations in the Zambezi Valley. PhD thesis. University of Zimbabwe, Harare. Debbie, Steve Vrdoljak and staff at Wildtracks as well as GRAHAM,A.(1968) The Lake Rudolf Crocodile (Crocodylus niloticus Reginald Mfula and staff at Kwalata Lodge for accommo- Laurenti) Population. A Report to the Kenya Game Department by dation and support, the lodges and people of the Lower Wildlife Services Ltd. Kenya Game Commission, Nairobi, Kenya.

HARTLEY, D.D.R. (1990) A survey of crocodile nests in Umfolozi Game SEIJAS, A.E. & CHAVEZ,C.(2000) Population status of Reserve. The Lammergeyer, 41, 1–12. the Orinoco crocodile (Crocodylus intermedius) in the HUTTON, J.M. (1984) Population Ecology of the Nile crocodile, Cojedes river system, Venezuela. Biological Conservation, Crocodylus niloticus, Laurenti 1768, at Ngezi, Zimbabwe. 94, 353–361. PhD thesis. University of Harare, Harare, Zimbabwe. SIAMUDAALA, V.M., KUNDA,C.&NAMBOTA, A.N. (2004) The Nile HUTTON, J.M. (1987) Morphometrics and field estimation of the size crocodile (Crocodylus niloticus) farming industry in Zambia. of the Nile crocodile. African Journal of Ecology, 25, 225–230. Game & Wildlife Science, 21, 853–863. HUTTON, J.M. & WOOLHOUSE, M.E.J. (1989) Mark recapture to assess SMITH, A.M.A. & WEBB, G.J.W. (1985) Crocodylus johnstoni in the factors affecting the proportion of a Nile crocodile population seen Mckinlay River area, N.T. VIII. A population simulation model. during spotlight counts at Ngezi, Zimbabwe, and the use of spotlight Australian Wildlife Research, 12, 541–554. counts to monitor crocodile abundance. Journal of Applied Ecology, SWANEPOEL, D.G.J., FERGUSON, N.S. & PERRIN, M.R. (2000) 26, 381–395. Nesting ecology of Nile crocodiles (Crocodylus niloticus) HUTTON, J.M., ROSS, J.P. & WEBB,G.(2002) Using the market to in the Olifants River, Kruger National Park. Koedoe, 43, create incentives for the conservation of crocodilians: a review. In 35–46. Crocodiles: Proceedings of the 16th Working Meeting of the IUCN/ TELLERIA, J.L., GHAILLANI, H.E.M., FERNANDEZ-PALACIOS, J.M., SSC Crocodile Specialist Group, pp. 382–399. IUCN, Gland, BARTOLOME,J.&MONTIANO,E.(2008) Crocodiles Crocodylus Switzerland. niloticus as a focal species for conserving water resources in KOFRON, C.P. (1989) Nesting ecology of the Nile crocodile Mauritanian Sahara. Oryx, 42, 292–295. (Crocodylus niloticus). African Journal of Ecology, 27, 335–341. THORBJARNARSON, J.B. (1996) Reproductive characteristics of the KOFRON, C.P. (1990) The reproductive cycle of the Nile crocodile order Crocodylia. Herpetologica, 52, 8–24. (Crocodylus niloticus). Journal of Zoology, 221, 477–488. THORBJARNARSON, J.B., WANG, X.M., MING, S., HE, L.J., DING, Y.Z., LAINEZ,D.(2008) Fifty years of crocodile surveys in Africa: a review WU, Y.L. & MCMURRY, S.T. (2002) Wild Populations of the of the surveys and population trends. MSc thesis. University College Chinese alligator approach extinction. Biological Conservation, London, London, UK. 103, 93–102. MACIEJEWSKI,K.(2006) Temperature-dependent sex determination TUCKER, A.D. (2001) Sensitivity Analysis of Stage-structured in the Nile crocodile Crocodylus niloticus in the Okavango River, Demographic Models for Freshwater Crocodiles. Surrey Beatty Botswana, and the effect of global climate change. MSc thesis. & Sons, Chipping Norton, Australia. University of Stellenbosch, Stellenbosch, South Africa. VELASCO, A., COLOMINE, G., DE SOLA,R.&VILLARROEL,G. MAZZOTTI, F.J., BEST, G.R., BRANDT, L.A., CHERKISS, M.S., (2003)Effects of sustained harvests on wild populations of JEFFERY, B.M. & RICE, K.G. (2009) Alligators and crocodiles as Caiman Crocodilus crocodilus in Venezuela. Interciencia, 28, indicators for restoration of Everglades ecosystems. Ecological 544–548. Indicators, 9,S137–S149. WEBB, G.J.W. & MESSEL,H.(1977) Crocodile capture techniques. MCGREGOR,J.(2005) Crocodile crimes: people vs wildlife and the Journal of Wildlife Management, 41, 572–575. politics of postcolonial conservation on Lake Kariba, Zimbabwe. WEBB, G.J.W., BRITTON, A., MANOLIS, C., OTTLEY,B.&STIRRAT,S. Geoforum, 36, 353–369. (2000) Recovery of saltwater crocodiles (C. porosus) in the Northern MILLS, L.S., DOAK, D.F. & WISDOM, M.J. (1999) Reliability of Territory of Australia: 1971–1998.InCrocodiles: Proceedings of the conservation actions based on elasticity analysis of matrix models. 15th Working Meeting of the Crocodile Specialist Group, pp. 195–234. Conservation Biology, 13, 815–829. IUCN, Gland, Switzerland. PARKER,I.&WATSON,R.(1970) Crocodile distribution and status in the major waters of western and central Uganda in 1969. East African Wildlife Journal, 8, 85–69. Biographical sketches POOLEY, A.C. (1969) Preliminary studies on the breeding of the Nile crocodile Crocodylus niloticus, in Zululand. The Lammergeyer, K EVIN M. WALLACE and A UDREY S. WALLACE have been involved 10, 22–44. with crocodile research for 7 years. Kevin has a wide interest in ecology R DEVELOPMENT CORE TEAM (2008) R: A Language and and wildlife conservation management. A LISON L ESLIE’ S research Environment for Statistical Computing. R Foundation for interests are wildlife ecology, vertebrate physiology and aquatic Statistical Computing, Vienna, Austria. Http://www.R-project.org conservation. She is particularly interested in the ecology and [accessed 19 April 2013]. conservation of crocodiles and sea turtles. T IM C OULSON’ S research RON, S.R., VALLEJO,A.&ASANZA,E.(1998) Human influence on the concentrates on how demographic rates vary across groups of wariness of Melanosuchus niger and Caiman crocodilus in individuals and environments, and the ecological and evolutionary Cuyabeno, Ecuador. Journal of Herpetology, 32, 320–324. consequences of this variation.