CCAMLR Science, Vol. 18 (2011): 75–114 A REVIEW OF THE DIET AND AT-SEA DISTRIBUTION OF PENGUINS BREEDING WITHIN THE CAMLR CONVENTION AREA N. Ratcliffe and P. Trathan British Antarctic Survey High Cross, Madingley Road Cambridge CB3 0ET United Kingdom Email – [email protected] Abstract Managing fisheries in an ecologically sensitive manner demands that catches do not depress stocks within the foraging areas used by predators to levels that reduce their reproductive success or survival. Spatially–explicit bioenergetics models that estimate the amount of prey consumed by predators are required to inform such policy. These models require information on the number of predators in a population, their nutritional demands, their diet composition and their seasonal distribution in the marine environment. This paper reviews all published information on the diet and at-sea distribution of the six penguin species that breed in the CAMLR Convention Area, the methods used to collect these data and the uncertainties inherent in them. The review will be of utility to modellers as a source of parameters, and to penguin biologists by providing comparative information for their own findings and by highlighting significant gaps in existing knowledge and methods that could be used to fill these. Introduction the models that relate to foraging ecology; namely their diet and at-sea distribution. Information of A key objective for CCAMLR is to estimate the distribution and size of penguin colonies and the biomass of different prey species consumed by predators, especially harvested species such as the energetic demands of penguins form the foci Antarctic krill (Euphausia superba) within each of of other strands of Subgroup on Status and Trend the management subareas of the Southern Ocean. Assessment of Predator Populations (WG-EMM- Quotas can then be set at levels that ensure that STAPP) work and will be presented elsewhere. stocks are not reduced to levels that will impact adversely on predator reproduction or survival. The review begins by giving an overview of Moreover, research interest is increasingly focusing methods for studying the diet and at-sea distribution on fine-scale spatial distribution of food consump- of penguins and a commentary on the uncertainties tion by predators in the marine environment. This associated with each approach. It then proceeds to facilitates spatially explicit fisheries management review all published information on the diet and that minimises the spatial overlap between predator at-sea distribution of the six penguin species that food consumption and fishery catches. The bioen- regularly breed within the CAMLR Convention ergetics models that produce estimates of total prey Area, broken down by division and subareas (for consumption require data on the number of indi- a map of these see www.ccamlr.org/en/organisa- viduals in a population, the energetic demands of tion/convention-area). Information from divisions each individual, and their diet composition (Boyd, outside the CCAMLR region (namely the Falkland 2002; Hill et al., 2007), while spatially explicit Islands and Macquarie Island) where three of the models require additional data describing the at-sea focal penguin species breed, is included in order distribution of the population. to ensure that the review is comprehensive. The review only includes published literature to allow the reader to check the information at source. In the Aims and scope case of the review of diet, studies that only present The aim of this review is to summarise published data on composition within a specific taxonomic data on penguins concerning the components of group (e.g. squid alone) are excluded. 75 Ratcliffe and Trathan The target audience of the review are penguin to recover solid constituents, and prey remains are biologists and ecological modellers. Penguin biolo- identified, counted and weighed. The main source gists will find the information in the review useful of uncertainty is that prey are often heavily digested for comparison with the findings of their own stud- when recovered, which may cause problems with ies, to identify important gaps in current knowledge identification and estimation of their original mass and to determine the most suitable methods that upon ingestion (Gales, 1987). However, some parts could be used to fill such gaps. Ecological model- of prey types resist digestion better than others and lers will be able to extract values of interest from have sufficiently unique characters to allow identi- the review and gain an improved understanding of fication to the level of genus or species. The beaks the uncertainties that may be associated with these. of squid, eye-capsules of crustaceans and sagittal Those readers wishing to extract large numbers otoliths of fish are particularly widely used in this of diet values may find it easier to do so from the respect. Counting these allows numbers consumed online spreadsheet compiled by Raymond et al. to be estimated, and original size of prey at diges- (2011). tion can be estimated from equations describing relationships between the size of the body parts and the whole body size, obtained from measurements Estimating diet composition of whole specimens captured in trawls (Hill et al., Quantification of prey remains 1996). The resulting corrections from such analy- in stomach contents ses are usually referred to as reconstituted mass, as opposed to wet mass measured from raw stomach Most diet studies of penguins are based on contents. Problems with this approach still remain, examination of the contents of the oesophagus, since erosion of these parts may result in underesti- proventriculus and gizzard, typically referred to mates of their numbers and size, and because these collectively (though anatomically inaccurately) as parts are digested at differing rates. For example, stomach sampling. The contents can be accessed by dissection, administration of emetics or by stomach fish components are digested particularly rapidly, flushing (also termed as water offloading, stomach while squid beaks are extremely resistant to diges- pumping or gastric lavage). Dissection involves tion and can accumulate in stomachs for several killing birds and cutting open the stomach to ex- days or even weeks, resulting in overestimates of tract its contents; this is the most thorough method the squid component (Pütz, 1995; van Heezik as all contents can be extracted (Croxall and Furse, and Seddon, 1989; Wilson et al., 1985). Most of 1980; Croxall and Prince, 1980; Volkman et al., the recent studies overcome the latter problem by 1980). This was only used in early studies of diet only counting those squid beaks still attached to the during the 1970s, and most researchers have sub- buccal mass. sequently considered it unjustifiable on ethical grounds. Emetics were also used in early studies Data derived from stomach content studies can (Jablonski, 1985; Volkman et al., 1980) but were be presented in three ways. The simplest method ineffective and their use has been discontinued. is percentage occurrence, which is the percentage Almost all studies since the mid-1980s have used of stomachs in which at least one prey item of a stomach flushing, in which a tube is inserted down given type is present. This tends to exaggerate the the oesophagus, down which warm water is poured importance of small food items that tend to occur until the stomach is full. The bird is then inverted in most stomachs but are never significant in terms over a bucket in which the regurgitated stomach of numbers or mass. Percentage by number is contents are collected (Gales, 1987; Wilson, 1984). the percentage of food items of a given type in a This procedure is often repeated for a fixed number stomach, and is usually averaged across stomach of times or until only clear water is returned, de- samples. This tends to exaggerate the importance pending on the study. The method does cause birds of numerous but small items and underestimates distress, and in exceptional cases results in death of the importance of large items, which are inevita- a study animal, but it is less intrusive than killing bly less frequent owing to limitations of stomach birds for dissection. volume. Percentage by wet mass or reconstituted mass are the percentage of the total mass of stom- Food recovered from stomachs is typically fil- ach contents comprised by a given prey type, and is tered through sieves with increasingly fine meshes the only measure that is of use in prey consumption 76 Review of diet and at-sea distribution of Convention Area penguins models. The estimates authors choose to present Fatty acid analysis often vary among studies, making direct compari- Different prey types often have unique types of son of values problematic. fatty acids, and predators consuming them will in- corporate these into their own blood and ultimately their adipose tissue or the yolk of their eggs (Raclot Quantification of prey remains in faeces et al., 1998; Tierney et al., 2008a). Sampling blood Faeces can be collected either ashore or on provides an assessment of prey consumed in the sea-ice or icebergs. Prey remains, such as squid previous couple of days and that in adipose tissue beaks, otoliths and crustacean eye-capsules can be over the previous month, offering varying tempo- identified and counted to quantify diet composition ral coverage and resolution. Blood samples can be (Green, 1986; Green et al., 1998). This method has taken from a vein using a hypodermic syringe, and adipose samples by fat biopsies or by dissection of the advantage that faeces can be collected relatively fresh cadavers. Samples need to be stored in chlo- easily and non-intrusively. However, the problems roform and methanol (in a 2:1 ratio) or frozen in a with digestion of prey and erosion of identifiable deep freezer or using liquid nitrogen (Tierney et al., parts described for stomach sampling are magni- 2008a).