© 2006 International Council for the Exploration of the Sea
A refined fish consumption model for lactating Cape fur seals (Arctocephalus pusillus pusillus), based on scat analyses
a Avian Demography Unit, Department of Statistical Sciences, University of Cape Town Rondebosch 7701, South Africa
b Lüderitz Marine Research, Ministry of Fisheries and Marine Resources PO Box 394, Lüderitz, Namibia
*Correspondence to S. Mecenero: tel: +27 21 6503648; fax: +27 21 6503434. e-mail: smecener{at}adu.uct.ac.za.
A refined fish consumption model for lactating Cape fur seals in Namibia during the eight-month lactation period, which allows for spatio-temporal variation in the diet as determined by scat analyses, has been developed. Previous estimates of prey consumption by Cape fur seals have been based mostly on coarse diet composition models. Sensitivity analyses showed that the energetic requirement and mass of lactating females (bioenergetic variables), as well as the energetic density of prey (diet variable), contributed most to the uncertainty in consumption estimates. Uncertainty in the remaining input variables had minimal effects on the estimates of food consumption. The consumption of commercial prey (horse mackerel, hake and pelagic fish) was greatest by the colony at Cape Cross. The model estimated that a female of average mass 55 kg ingested, on average, 11% of her body mass per day. This model is easily applied to other age/sex classes of the seal population. It permits improvement of the estimates of prey consumption by seals, which are useful for assessing levels of competitive interactions between seals and fisheries or other predators, or the impacts of seals on prey species.
Keywords: Cape fur seal, fish consumption, lactating females, model, Namibia, scat analysis, spatial variation, temporal variation
Received 6 May 2005; accepted 8 June 2006.
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Introduction |
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 Top Introduction Material and methodsResultsDiscussionReferences |
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In both South Africa and Namibia, the Cape fur seal (Arctocephalus pusillus pusillus) population is perceived by some as a competitive threat to the success of commercial fisheries (Wickens et al., 1992a). Subscribers to this point of view believe that increases in the size of the seal population negatively affect the catches of the fisheries. Their concerns have intensified in recent decades, because the fur seal population has increased at about 3% annually since 1971 (Wickens et al., 1991), despite substantial annual harvests of seals in Namibia (suspended in South Africa after 1990; Wickens and York, 1997). The Cape fur seals' total population size in Namibia was estimated at just over half a million individuals during a survey in December 2001 (Marine and Coastal Management, MCM, South Africa, unpublished data). Commercially important fish species preyed on by fur seals off Namibia (Mecenero et al., 2006a) include Cape horse mackerel (Trachurus trachurus capensis), Cape hake (Merluccius capensis and M. paradoxus), sardine (Sardinops sagax), anchovy (Engraulis capensis), and round herring (Etrumeus whiteheadi) (Shaughnessy, 1985).
In order to determine levels of competition for a prey resource between two or more groups of predators, it is necessary to estimate levels of consumption by each group (Harwood and Croxall, 1988). Previous studies have estimated consumption of the Cape fur seal population as the product of population size and the daily prey requirement of an individual of average size, the latter assumed to be a set percentage of body weight (Shaughnessy, 1985; Butterworth et al., 1988; Wickens et al., 1992b), or from an allometric equation for growing marine mammals (Wickens et al., 1992b; Balmelli and Wickens, 1994; Smale et al., 1994; Butterworth et al., 1995). The more refined of these studies incorporated information on the population age structure (Butterworth et al., 1995), or apportioned the total consumption into prey groups using information on diet composition obtained from analyses of stomach contents (David, 1987). However, none of these studies took into account the varying calorific content (or energy density) and the digestive efficiency (also known as the assimilation efficiency) of prey of different species, or variation in the diet composition between locations and over time, as has been demonstrated to be the case for Namibia's seal population (Mecenero et al., 2006a, b).
In this study, we develop a model that considers all these factors (except digestive efficiency, assumed to be the same for all teleost prey species), and base it on analyses of scat samples collected at three mainland breeding colonies in Namibia over a period of eight years. The model is limited to the teleost portion of the seals' diet, as this is the only component that can be quantified from scats, and only applies to lactating females, which were assumed to have deposited almost all the scats found at the colonies during the lactation period (Rand, 1959), which comprises the greater part of the year.
Female Cape fur seals attain sexual maturity at 3–4 years of age (Shaughnessy, 1985; David, 1995). Pregnant females start arriving at breeding colonies towards the end of October or early November and give birth to one pup soon afterwards (Rand, 1955; Shaughnessy, 1985). The bulk of pup production is in December (median pupping date 3–10 December; De Villiers and Roux, 1992). After giving birth, females alternate foraging trips to sea with suckling periods on land until the pup is weaned 8–10 months later (Rand, 1955; David, 1995).
Cape fur seals feed mainly over the continental shelf (David, 1987). Most dives are shallower than 50 m (Kooyman and Gentry, 1986) and half of the dives occur at night, becoming shallower as the night progresses, possibly in response to prey migrating to the surface during the night (David, 1995). Although information is limited, there are indications that there is movement between colonies in Namibia, and seals from different colonies certainly overlap in their foraging areas (Oosthuizen, 1991). The foraging range of Cape fur seals is within 220 km of their colony (Shaughnessy, 1985). Moreover, seals from South Africa do move north into Namibian waters, and some seals tagged in South Africa have been found as far north as northern Namibia (Oosthuizen, 1991). A few seals tagged in southern Namibia moved south into South African waters, but the general direction of movement is northwards (Oosthuizen, 1991).
Being generalist feeders in a highly variable ecosystem, Cape fur seals can be expected to feed on locally abundant prey species (Shaughnessy, 1985; Oosthuizen, 1991). This is particularly true for lactating females that are restricted in terms of the range that they can forage from their breeding colony. As central place foragers, their foraging distance from the colony is an important factor (Guinet et al., 2001), determined by the physiological limits of the mothers and the requirements of the pups (Beauplet et al., 2004). A lactating mother's trip duration is determined by the time taken to regain the energy lost during suckling and travelling (Costa et al., 1989). Gamel et al. (2005) found that trip lengths of lactating Cape fur seal females increased during the first four months of lactation. It is unknown whether increases in foraging trip lengths are caused by reduced local prey availability, or increasing independence on the part of the pups. In the case of Subantarctic (Arctocephalus tropicalis; Georges et al., 2000a, b; Beauplet et al., 2004) and Antarctic (Arctocephalus gazella; Bonadonna et al., 2000; Staniland and Boyd, 2003) fur seals, increases in trip duration by lactating females are apparently associated with longer distances travelled to foraging locations, suggesting the former.
The model used in this study takes account of temporal variation in prey consumption that is related to variation in both diet composition (detected in scat analyses) and seal population numbers, making this model more refined than previous models. This is appropriate, considering the environmental variability that characterizes the northern Benguela ecosystem (Shannon et al., 1992).
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Material and methods |
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Study sites
Scat samples were collected at three mainland breeding colonies of Cape fur seals in Namibia: Cape Cross (CC; 21°47'S 13°57'E), Atlas Bay and Wolf Bay (AWB; 26°49'S 15°08'E, and 26°48'S 15°07'E, respectively), and Van Reenen Bay (VRB; 27°23'S 15°21'E; Figure 1). Because of the close proximity of the Atlas and Wolf Bay colonies, which are about 1 km apart, they were considered to be a single colony for the purposes of this study. Together, these three colonies represent about 65% of Namibia's seal population.
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The study colonies are in regions that are distinct from each other in the northern Benguela (Figure 1). The three regions were defined as follows: Region 1 extended from the border with Angola (17°S) to Meob Bay (24°30'S), Region 2 from Meob Bay to just north of VRB (27°15'S), and Region 3 from just north of VRB to the border with South Africa (28°30'S; Figure 1). Meob Bay divides Regions 1 and 2, because there is a biological boundary in its vicinity (Agenbag and Shannon, 1988). The division between Regions 2 and 3 was placed just north of VRB around 27°S (near Lüderitz), the most intense upwelling centre of the Benguela ecosystem, characterized by strong winds and placed where the continental shelf is narrowest and deepest (Shannon, 1985). This upwelling cell effectively divides the Benguela into two and acts as a virtually perennial barrier to the movement of small pelagic fish (Shannon, 1985; Bianchi et al., 1993), which are the main constituents of seal diet. Although seals obviously do not respect political boundaries (Oosthuizen, 1991), the regions are within the northern and southern boundaries of Namibia, so the consumption estimates are comparable with Namibian fishery catches. Moreover, the Angola–Benguela front, which is situated off southern Angola around the boundary with Namibia, separates the tropical Angola Current from the cool Benguela Current (Shannon, 1985).
Study period
Scats were collected from January 1994 to April 2002. The lactation period was assumed to be from 1 December (the peak of the breeding season) to 31 July of the following year. This is because pups start being weaned after July (Rand, 1955) and, at CC and AWB, the onset of commercial seal harvesting then results in lactation being terminated for a substantial number of the mother–pup pairs. The annual pup harvests at CC and AWB were as high as 25 000 and 19 000 pups, respectively, during the study period (Ministry of Fisheries and Marine Resources, MFMR, Namibia, unpublished data).
We intended to collect scats on a monthly basis during the lactation period, but logistical constraints meant that none of the colonies could be visited every month. Of the 72 months constituting the nine lactation periods over the entire study period, CC was sampled during 49, AWB during 64, and VRB during 31.
Collection and processing of scats
Only fresh scats, less than approximately two days old, were collected by walking through the colony with minimal disturbance to the animals. A month's sample of scats constituted a bag of 30–60 pooled scats. Samples were stored at –10°C until processed.
The scat processing procedure is detailed in Mecenero et al. (2006a). Briefly, scat bag samples were washed in water, and the remaining material was passed through nested stainless steel laboratory test sieves with mesh apertures of 2.0, 1.0, 0.425, and 0.212 mm, then dried overnight in an oven at 50°C. Teleost sagittal otoliths were sorted from the dried matter, identified to the lowest possible taxon, and counted. Six teleost prey groups were identified, namely Cape hake, Cape horse mackerel, pelagic goby (Sufflogobius bibarbatus), lanternfish (mainly Lampanyctodes hectoris), pelagic fish (sardine, anchovy, and round herring), and other teleost species (Mecenero et al., 2006a).
Otolith counts were corrected for numbers lost during digestion using correction factors (for a full account of the values used, see Mecenero et al., 2006a), which were determined by captive feeding trials (D. L. Millar et al., MCM, unpublished data). The otolith diameters of monthly subsamples of otoliths from each prey group were measured to the nearest 0.05 mm for each month. Otolith diameters were corrected for erosion using correction factors (Mecenero et al., 2006a; D. L. Millar et al., unpublished data), then converted to fish mass using species-specific relationships between otolith diameter and fish total length and mass (Smale et al., 1995; Mecenero et al., 2006a).
For each monthly sample at each colony, the median fish mass for any given teleost prey group was multiplied by the group's corrected otolith counts for that month, to estimate the total mass of each group in a sample. To standardize for differences in sample sizes, the estimated mass of each prey group present in a monthly sample was expressed as a proportion of the estimated mass of all prey groups in that sample (Mecenero et al., 2006a).
Prey consumption model
The model used to estimate the daily consumption of teleost prey by lactating Cape fur seals during the lactation period at each study colony follows that of Winship et al. (2002) and Goldsworthy et al. (2001), and includes correction factors for the efficiency of converting prey energy to digestible energy (Doidge and Croxall, 1985; Goldsworthy et al., 2001):
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| (1) |
The mass requirement for prey group i (MRi; t) by lactating Cape fur seals for each eight-month lactation period was estimated as follows:
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| (2) |
Prey consumption for lactating females was estimated for eight of the nine lactation periods within the study period. The exception was 1993/1994 (December 1993 to July 1994) because that period was characterized by mass mortality of pups (about 95% mortality) and high mortality of adults (about 300 000 seals) as a result of a warm water event which saw warm water coming south into the Benguela ecosystem from the north (Roux, 1998).
Estimates of prey consumption for lactating females at the study colonies were extrapolated to the entire subpopulations of lactating females falling within the three regions defined above. Thereby, an estimate of prey consumption was obtained for that portion of the Namibian population of Cape fur seals during the eight-month lactation period.
Estimates of the total consumption of commercial prey (hake, horse mackerel, and pelagic fish) by lactating females during the lactation period were derived by extrapolating the consumption estimates of those three commercial prey groups at each colony to the subpopulations within each of the three regions, then obtaining the total consumption of each prey group for the entire region of Namibia for each lactation period. To place the consumption of commercial prey by lactating females during the lactation period in context, relative to fishery landings, the consumption of commercial prey during each year's lactation period was expressed as a percentage of the total annual fishery landings.
Model inputs
Diet composition
Teleosts have previously been reported to constitute 92–97% of the diet of seals in Namibia (David, 1987; Lipi
ski and David, 1990), so for this study it was assumed that they accounted for 95% (T) of the diet, on average.
The proportion of the monthly relative mass of each teleost prey group at each study colony was used to estimate propim. This was based on the sorting, counting, and measurement of otoliths from the scat samples, and the conversion of abundance of respective prey items in the samples to mass, as described above. For months where values were missing, owing to the variation in sampling effort between study colonies, missing values within a lactation period were estimated by taking the average of values within the same lactation period. For the lactation period 1996/1997 at VRB, no diet data were available, so monthly missing values were estimated by taking the average of the corresponding months in the preceding and succeeding lactation periods at VRB.
The monthly relative percentage mass of each teleost prey group in the seal diet at each study locality during each lactation period is given in Mecenero et al. (2006b). Detailed examination of temporal variability (annual, seasonal, and monthly) in diet composition showed that the diet displayed significant inter- and intra-annual variation, with little seasonality (Mecenero et al., 2006b). However, some prey species displayed some seasonal patterns, possibly as a result of their life history, e.g. lanternfish and goby at AWB, and horse mackerel at CC.
Energetic density of prey
The mean (±s.d.) calorific content (wet mass, kJ g–1), or energetic density (ED), of Cape fur seal prey items as presented by Balmelli and Wickens (1994) was used: Cape horse mackerel, 5.65 ± 0.80 kJ g–1; Cape hake, 4.47 ± 0.57 kJ g–1; lanternfish, 4.90 ± 0.80 kJ g–1; pelagic goby, 3.69 kJ g–1 (no s.d.); pelagic fish, 6.18 ± 0.36 kJ g–1 (the average of sardine 6.59 kJ g–1, anchovy 6.03 kJ g–1, and round herring 5.91 kJ g–1); and others, 4.98 ± 0.60 kJ g–1 (average of the previous five prey groups). The ED of prey species varies seasonally (Balmelli and Wickens, 1994; Rosen and Trites, 2000), with geographic location and with prey age class (Rosen and Trites, 2000). This variation in calorific content was disregarded in the model, because it is currently unknown for species in this area.
Digestive efficiency
The digestive efficiency (DE) of fish consumed by fur seals has previously been documented as 93% by Miller (1978), while that of fish fed to captive juvenile Steller sea lions (Eumetopias jubatus) was reported to range from 92 to 96% (Rosen and Trites, 2000). For this study a DE of 93% (i.e. 0.93) was assumed for all prey. Although DE increases with the energy density of prey (Rosen and Trites, 2000), and may vary with predator age (Harper, 1998), this variation has not been quantified for Cape fur seals and their prey, so was not considered in the model.
Energy requirement of lactating females
The daily at-sea energy requirement (ERat-sea) of Cape fur seals was previously estimated to be 7.0 W kg–1 for a female of mass 68 kg (Gentry et al., 1986). However, the equation that was used (Gentry et al., 1986) was based on the northern fur seal, a sub-polar species that is somewhat smaller (females, 30–50 kg) than the Cape fur seal (females, 40–110 kg). In the absence of any relationship specific to Cape fur seals, a relationship supplied by Goldsworthy et al. (2003) was considered an improvement to that by Gentry et al. (1986), in that it was based on studies of seven otariid species, ranging in size and geography:
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| (3) |
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The ERat-sea for lactating northern fur seals (Callorhinus ursinus) (Costa and Gentry, 1986) and for Antarctic fur seals (Costa et al., 1989) was 1.8 and 1.9 times greater, respectively, than their on-shore energy requirements (ERon-shore). Both Antarctic and northern fur seals inhabit cold waters of sub-polar regions (Bonner, 1994). Krill is the main prey of Antarctic fur seals (Reid and Arnould, 1996; Kirkman et al., 2000; Casaux et al., 2003), although myctophids also form a substantial component of the diet (Cherel et al., 1997; Klages and Bester, 1998; Lea et al., 2002). Like Cape fur seals, northern fur seals feed mainly on schooling fish (Perez and Bigg, 1986). Accordingly, the ratio between at-sea and on-shore ER for northern fur seals was assumed to apply to Cape fur seals, so the daily ERon-shore for each adult female age class was estimated.
According to Costa and Gales (2000) and Winship et al. (2002), the total daily energy requirement (ER) of lactating female seals is determined as
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| (4) |
Lactating Cape fur seals spend 39% of their time on shore during the lactation period (Gentry et al., 1986). The daily ER for lactating Cape fur seals for each age class is given in Table 1.
Numbers, age structure, and mass of lactating females
Pup production at each study colony, as determined from aerial surveys conducted in the third week of December for five of the eight lactation periods (1994/1995, 1995/1996, 1996/1997, 1997/1998, and 2001/2002) (Johnston et al., 2004), was assumed to represent the number of females lactating at that colony in December of that year (Table 2); females give birth to one pup only (Rand, 1955). For years without an aerial survey (1998/1999, 1999/2000, and 2000/2001), pup counts were estimated by linearly interpolating between the available counts of the preceding and succeeding years. Adjustments were made for pup mortality over the period December–July; in January, pup mortality was assumed to be 30% (27–32%) of pup production, and for February–July 32% (27–34%) of pup production (MFMR, unpublished data). The age distribution and mass of lactating Cape fur seals from age 4 years onwards (Table 1) was used to estimate Nym and wy, respectively, in Equation (1).
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The number of pups born at colonies outside the study colonies within each of the three regions was determined by aerial surveys conducted at the same time as those for the study colonies. These colonies included (Figure 1): four in Region 1, eight in Region 2, and three in Region 3. Thus, the proportion of pups born at each study colony within each region was estimated.
Uncertainty estimates
Uncertainty estimates for model outputs (MR, the mass requirement over the lactation period) were determined following existing randomization and bootstrap methods (Hammond and Rothery, 1996; Boyd, 2002; Winship et al., 2002; Winship and Trites, 2003). For each of the MR estimates, errors were determined by iterating the model 1000 times using values randomly selected from distributions that described the uncertainty in the input values: the normal distribution was used if the input value was defined by a mean and standard deviation (EDi and wy); the uniform distribution was used if the input value fell within a range (upper and lower limits) of available plausible values (T and DEi); the triangular distribution was used for input values defined by a median and range (pup mortality and propim). For propim values, between-sample variability associated with scats constituting a month's sample could not be determined, because each month's sample consisted of pooled scats. Instead, within-sample variability was used by determining the variability associated with estimates of fish mass derived from measurements of subsamples of otoliths within each month's sample (Mecenero et al., 2006a). No estimates of variability were available for numbers of lactating females (Nym), because these counts were based on once-off counts of pups from aerial photographs, and for the age distribution because those values were derived from a separate study (Butterworth et al., 1995) that did not provide measures of error. Each run of the model produced a consumption estimate for the lactation period (MR). Uncertainty estimates (95% confidence intervals) were determined by taking the 2.5th and 97.5th percentiles for each set of 1000 iterations. Uncertainties in the consumption estimates are related to natural variability and measurement error (Boyd, 2002).
Sensitivity analyses
Sensitivity analyses were conducted to determine the extent to which variability in each input variable, and groups of variables, contributed towards explaining the variance in the food consumption estimates, following existing randomization and bootstrap methods (Hammond and Rothery, 1996; Boyd, 2002; Winship et al., 2002). To do this, consumption estimates were determined for all prey groups, study colonies, and lactation periods combined. Confidence intervals for each sensitivity test were determined by iterating the model 1000 times and taking the 2.5th and 97.5th percentiles. To determine the sensitivity in relation to each input variable (or group of input variables), we calculated the ratio of the length of the confidence interval for each input variable (or group) to the length of the confidence interval for the model when all input variables were random.
Sensitivity was calculated for (i) each input variable separately while maintaining all other input variables constant, (ii) three groups of input variables separately while the remaining groups were kept constant, where the groups were defined as the diet (T, EDi, and propim), bioenergetic (DEi, ERy, and wy), and population (pup mortality) groups, and (iii) pairs of groups while maintaining the third group constant, to determine the interactive effects between all possible pairs of groups. The sensitivity of the model to variability in ERy and wy was calculated with the two variables inclusive, because ERy is influenced by wy (see Equation (3)).
Additionally, because pup counts may have been underestimated as a result of pups being hidden by shadows or rocks in the photographs (Shaughnessy, 1987), the effect of a 10% underestimate in the numbers of females (Nym) in model outcomes was determined for the model when all input variables were expressed with uncertainty, as well as for uncertainty associated with the population group and for pairs of groups that contained the population group.
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Results |
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Sensitivity analyses
Of the six input variables investigated separately (models 2–7; Table 3), food consumption estimates were most sensitive to uncertainty in the energetic density of prey (ED) and the daily energetic requirements of lactating females together with female mass (ER + w), contributing 51–78% to the overall variability (Table 3). Of the three groups of input variables (models 8–10; Table 3), diet and bioenergetic groups contributed most to the variability in consumption estimates, the contribution of the bioenergetic group being highest (78%). Pairs of groups containing the bioenergetic group (models 11 and 12; Table 3) also contributed highly to the uncertainty in consumption estimates (81–97%). Uncertainty in the proportion of teleost prey groups in the diet (propim), the total proportion of teleost fish in the diet (T), digestive efficiency (DE), and pup mortality contributed minimally (6–13%) to the variability in food consumption estimates (Table 3).
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Increasing the number of lactating females (Nym) by 10%, to incorporate an underestimation in pup count numbers, did not have a large effect on the model outcomes (Table 3). For the model where all input variables were expressed with uncertainty, it increased variability by 11%, and for the relevant sensitivity models (models 10, 11, and 13), it increased variability by 2–9%.
Food consumption
At each colony, the estimated intake of teleosts by lactating fur seals during the lactation period varied between years (Table 4). Over the eight years of the study, estimated annual prey consumption by lactating females during the period December–July ranged between 26 809 and 41 936 t at CC, 26 433 and 87 979 t at AWB, and 2832 and 5367 t at VRB. At all three colonies, annual consumption was highest in the lactation period of 1997/1998. Combining estimates for the three colonies, teleost prey consumption ranged from 58 736 (1994/1995) to 135 282 t (1997/1998; Table 4). The annual total consumption of teleost prey by lactating seals in the whole of Namibia was estimated to range between 90 000 and 185 000 t (Table 5). On average, lactating seals in Region 2 consumed 54% of all teleosts consumed, whereas seals in Regions 1 and 3 consumed 32% and 14%, respectively.
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The proportional representation of the different teleost prey groups in the estimates of consumption varied between years at each colony (Table 4). Commercial prey accounted for a large proportion (74–99%) of the total teleost mass consumed at CC, whereas at AWB and VRB commercial prey constituted low to high amounts of the total prey consumed (16–80% and 25–86%, respectively; Table 4). For the three colonies combined, commercial prey represented 47–78% of the total teleost mass consumed.
Assuming an average mass of 55 kg for lactating seals, and estimating the daily mass ingested per individual seal for each lactation period at the study colonies, then on average each lactating seal ingested 10 ± 1% (mean ± s.d.) of its body mass per day (95% confidence interval, 8–13%; n = 24).
Comparisons with commercial fisheries
The estimated annual consumption of horse mackerel by lactating female Cape fur seals in Namibia during the lactation period amounted to just 2–13% of fishery landings (Table 6). By comparison, the consumption of hake was 12–80% of fishery landings and of pelagic fish 4–69% (Table 6).
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Discussion |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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Assessing levels of competition for a prey resource between two or more groups of predators requires that levels of consumption by each group first be estimated (Harwood and Croxall, 1988). In this study, dietary information from analysis of scats collected at three mainland breeding colonies in Namibia, over eight years, was used to develop a model of prey consumption by a component of the country's seal population, namely lactating females. The model was limited to lactating females, because it could easily be assumed that they deposit the majority of scats at breeding colonies during the lactation period. As the same cannot be assumed for the period between weaning and the commencement of the next season of birth, this period was excluded. Also, the model is limited to the teleost portion of the seals' diet, as this is the only component that can be re-constructed from scat remains.
Whereas some of the previous models of prey consumption by Cape fur seals (e.g. Shaughnessy, 1985; David, 1987) assumed diet to be uniform, the model developed in this study incorporated spatial and temporal variation in diet composition that was apparent over the eight-year study period at three different colonies. Additionally, previous consumption estimates for the Cape fur seal (Shaughnessy, 1985; David, 1987; Butterworth et al., 1988, 1995; Wickens et al., 1992b; Balmelli and Wickens, 1994; Smale et al., 1994) did not incorporate the energetic density and the digestive efficiency of the different prey species. The finer resolution of this model provides estimates of variability in consumption, by incorporating uncertainty in the model's input parameters. An understanding of this variability is important when using models for fisheries management (Tollit and Thompson, 1996). Moreover, taking variability into account is appropriate, considering the great variability of the northern Benguela (Shannon et al., 1992).
The consumption estimates obtained were not extrapolated to the entire seal population (all sex/age classes) of Namibia because the diet of seals varies within species according to sex, age, and reproductive stage (Lowry et al., 1980; Acuña and Francis, 1995; Lawson et al., 1995; Casaux et al., 1998; Mikkelsen et al., 2002). Specifically, there are gender differences in diet composition of Cape fur seals (Castley et al., 1991), likely a consequence of gender differences in both energy requirements and ranging behaviour (Pierce and Boyle, 1991). The usefulness of a model that is limited to a portion of the population for a portion of the year might be questioned. However, the aim of this exercise has primarily been to develop an improved model for estimating consumption by seals. The model can be applied easily to other age/sex classes of the seal population, and to other seal species, if the necessary data are available.
To extrapolate the consumption estimates determined for each study colony to their regions, it was assumed that the diet at each study colony represented the diet of seals in each region, respectively, and that foraging ranges did not overlap between regions. These assumptions may not hold, because fish distributions may vary within regions. Moreover, seals from colonies at the edges of the regions may forage in adjacent areas.
The consumption model in this study is based on the assumption that the daily mass requirements of a seal are fulfilled. Therefore, the annual total consumption of teleosts would be overestimated for years of high mortality through starvation or other reasons, for which reason the lactation period of 1993/1994 was excluded from the model. In at least two other years, high pup mortality and poor body condition among adults were observed, though not on the scale of 1994 (J-PR, unpublished data). These were 1995, a Benguela Niño year, and 1999, a warm water event (Hardman-Mountford et al., 2003) similar to that of 1994 (Roux, 1998). The model may therefore overestimate teleost consumption in those years.
The model uses information retrieved from scat samples to estimate consumption, and is therefore subject to the many weaknesses inherent in the use of scats for diet studies (Pierce and Boyle, 1991). For example, small otoliths can be completely eroded during digestion, and otoliths that are retrieved have undergone a degree of erosion during digestion, affecting estimates of fish length from otolith diameter. The effects of digestion on otolith numbers and size were corrected for in this study using conversion factors determined during captive feeding trials on Cape fur seals (D. L. Millar et al., MCM, unpublished data). These contributed to a more reliable estimate of fish mass in the diet (Harvey, 1989; Staniland, 2002). Also, while the relative importance of different teleost prey can be estimated from the information contained in scats, it is impossible to estimate the relative importance of teleosts to other prey groups such as cephalopods, crustaceans, and seabirds. Seabird and crustacean remains found in scats comprise mainly feathers and crushed carapace, respectively (SM, pers. obs.), allowing for little more than detection of their occurrence, whereas differences in retention rates of otoliths and cephalopod beaks means that information obtained from those two types of prey remains are not directly comparable (Pierce and Boyle, 1991; Gales and Cheal, 1992). Based upon previous analyses of stomach contents (David, 1987; Lipiski and David, 1990), it was assumed for the model that teleosts constitute 95% of the diet of seals in Namibia. It is probable, however, that the intake of teleosts relative to other prey groups changes with time and location. For example, scats found at a non-breeding locality north of AWB (Sylvia Hill, 25°08'S 14°50'E) contained almost 100% crustaceans (SM, pers. obs.).
The annual consumption estimates varied greatly, possibly reflecting life-history patterns of some of the prey, or changes in prey distribution and abundance in response to the highly variable environmental conditions of the Benguela (Mecenero et al., 2006b). Moreover, the wide confidence intervals reflect a large degree of uncertainty in the consumption estimates, which are related to the assumed errors for some of the input variables.
The estimates of food consumption were most sensitive to uncertainty in the daily energetic requirements and the mass of lactating females (i.e. the bioenergetic variables). This study's model would be improved if the actual energetic requirements of lactating Cape fur seals were determined, for instance by conducting energetic studies on free-ranging seals using double-labelled water methods (e.g. Costa and Gentry, 1986; Costa and Gales, 2000; Trillmich and Kooyman, 2001). The energetic requirements of Cape fur seals should take into account the energy required and the amount of time spent both at sea and on shore (Costa et al., 1989; Costa and Gales, 2000; Goldsworthy et al., 2001). In this study, the at-sea energy requirements of lactating Cape fur seals were based on a scaling equation (Gentry et al., 1986). Following this, on-shore energy requirements were determined by using the factor of difference between the at-sea and on-shore energy requirements of northern fur seals. However, there are differences in lactating, diving, and foraging behaviour, as well as in average body size, between Cape and northern fur seals. Such variation would likely influence the difference between at-sea and on-shore energy requirements (Doidge and Croxall, 1985; Innes et al., 1987; Costa et al., 1989). The energy requirements of seals vary by sex, age, and reproductive status (Laake et al., 2002), and these factors should also be taken into account in consumption models.
Additionally, food consumption estimates were sensitive to uncertainty in the energetic density of prey. The variation in calorific content of prey related to season, location, and prey age class (Rosen and Trites, 2000) should be determined for the main prey of the seals, in order to minimize their contribution to uncertainty in the model.
Information on the efficiency of digestion of prey by different sex/age classes of Cape fur seals is lacking, so an assumption had to be made in this regard for lactating females, based on other studies. Digestive efficiency may vary with sex and age of the seal, and with prey type and calorific content (Rosen and Trites, 2000). Further, the calorific content of prey may vary seasonally, geographically, and with age (Rosen and Trites, 2000). Although the digestive efficiency of prey contributed minimally to the uncertainty in the consumption estimates, captive feeding trials including variation in prey type and the sex/age class of seals may allow for a more informed estimate in this regard.
This study determined that, on average, lactating females ingested 10% of their body mass per day. This becomes 11% after correction for the non-teleost proportion of the diet (assumed to be 5%). In other words, a lactating female of average size (55 kg) consumed an average of 6 kg d–1 (range 4–8 kg d–1, n = 24). This value falls within the daily energy requirements for other otariids, which range from 5% (Steller sea lion; Winship et al., 2002) to 23% (Antarctic fur seal; Doidge and Croxall, 1985) of body mass. The consumption models of Wickens et al. (1992b) and David (1987) assumed that the daily prey requirement of lactating Cape fur seals was 10% and 8% of body mass, respectively, similar to the value estimated in this study. A similar estimate was produced using the allometric equation of Innes et al. (1987) for growing marine mammals. Using that equation, Balmelli and Wickens (1994) and Smale et al. (1994) estimated that an individual Cape fur seal consumed 4 kg d–1, making no distinction between seal sex/age classes.
The estimated consumption of commercial prey was greatest at CC. This was due to the abundance of hake and juvenile horse mackerel remains in the scats collected there (Mecenero et al., 2006a). Juvenile horse mackerel are mainly found along the northern coast of Namibia in the vicinity of CC (Krakstad and Kanandjembo, 2001). At AWB and VRB, the two colonies on the southern coast of Namibia, consumption of horse mackerel was low due to its limited abundance in the region (Axelsen et al., 2004). For seals from those colonies, non-commercial species such as goby and lanternfish were more common in the diet (Mecenero et al., 2006a).
Although this study only looks at a part of the seal population (lactating females) and a fraction of the year (lactation period), comparisons of the quantity of commercial prey consumed with those taken by fisheries showed that lactating females consumed relatively small amounts of horse mackerel in relation to the annual landings of horse mackerel. Hake and pelagic fish consumption by lactating seals relative to fishery landings was higher, sometimes exceeding fishery catches. However, although seals and fisheries utilize the same commercial prey resources, this does not automatically imply that there is competition between them. To determine the extent to which competition exists between seals and fisheries, additional information is required, such as fish distribution and abundance, feeding effort, amount of fish utilized and size classes utilized by seals and fisheries in time and space, the response of fish to changes in predation rate, the response of seals, fisheries, and other predators to changes in fish abundance, and the response of the market to fish supply (Harwood and Croxall, 1988; Green et al., 1998). For example, seals generally consumed smaller horse mackerel than those taken by the purse-seine fishery (Mecenero, 2005). Unless all this information, which is usually difficult to obtain, is available, competition between two resource utilizers cannot be determined effectively.
Differences in amounts of commercial species caught by fisheries and consumed by seals can be affected by the distribution of the stock, which in turn is influenced by changes in environmental conditions and food availability (Shannon et al., 1992). For example, although the calculated biomass of the horse mackerel stock in 2001 and 2002 was similar (
850 000 t; Bauleth-D'Almeida et al., 2001; Krakstad et al., 2002), the 2001 stock was more widely distributed in northern waters of Namibia, encompassing CC, and consisted of smaller fish (<17 cm) than the 2002 stock, which consisted of larger fish (>17 cm) and was concentrated in the north near Cape Frio (18°30'S; Bauleth-D'Almeida et al., 2001; Krakstad et al., 2002). Consequently, the 2002 horse mackerel stock was largely inaccessible to lactating seals at CC, as it was largely outside their foraging range, and this was reflected in the lesser proportional consumption of horse mackerel in 2002 compared with the fishery.
The model developed in this study provides an improved estimate of prey consumption by Cape fur seals, more specifically for lactating individuals. By improving estimates of prey consumption, better understanding can be obtained regarding competition between consumers of a common resource (Harwood and Croxall, 1988), in this case seals and fisheries competing for commercial fish stocks. Using well-planned captive feeding trials, better estimates of some of the model parameters will be obtained, which will make the model more accurate and so provide a better understanding of the interactions between seals, their prey, and the fisheries.
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Acknowledgements |
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This study is part of the Namibian Ministry of Fisheries and Marine Resources' (MFMR) ongoing investigation of the diet of the Cape fur seal population in Namibia. The seal diet sampling and processing was undertaken by researchers and technicians of the Marine Mammal Section at MFMR, and the Pelagic and Demersal Sections assisted in collecting samples at Cape Cross; special thanks go to Kleophas Tangeni Kleophas and Ndako Mukapuli. Logistical support was provided by MFMR. The project was supported by a National Research Foundation (NRF) prestigious bursary to SM. We thank Les Underhill (Avian Demography Unit, Department of Statistical Sciences, University of Cape Town, South Africa) and Rob Crawford (Marine and Coastal Management, South Africa), and two anonymous referees, for their comments on earlier drafts of the manuscript.
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