Foraging behavior of Brazilian cormorant , Nannopterum brasilianus ( Suliformes : Phalacrocoracidae )

Although the concept of optimal foraging has been extensively discussed, foraging efficiency is difficult to assess in vertebrates. In this study, we determined the foraging efficiency of the Brazilian cormorant, Nannopterum brasilianus Gmelin, 1789, by the direct, ad libitum observation of a group of four to thirteen individuals in an artificial pond at the University of São Paulo, Piracicaba, state of São Paulo, southeastern Brazil. Although this study was carried out in a highly anthropic environment, we can still conclude that the Brazilian cormorant is a relatively efficient browser and short-term diver. In anthropic environments, foraging success depends on the amount of time these birds spend diving, and stealing food is less common. Stealing occurs at relatively low rates but tends to be an efficient way to get food.


INTRODUCTION
Even though most will agree that measuring animal behavior in the context of experimental research helps to decrease the subjectivity of observations (Martin and Bateson 1993), descriptive studies -formerly called "naturalistic observations" (Lehner 1979(Lehner , 1996) ) -can also help to give a preliminary understanding of a species' natural history, and often generates hypotheses that will lead to experimental research (Bakeman and Gottman 1986).In addition, even preliminary descriptions of behaviors can be quantified.
Although optimal foraging has been extensively discussed (Krebs 1978, Stephens and Krebs 1986, Crawley and Krebs 1992, Alcock 1993, Krebs and Davies 1993), foraging success rate has rarely been determined in vertebrates (Schaller 1972).The reason for this is that it is necessary to describe foraging qualitatively and quantitatively.Predators are rarely conspicuous, and predation usually involves disguise and concealment (Caro andFitzGibbon 1992, Guilford 1992).In addition, successful predation is not as frequent as one might suppose.
Cormorants are usually one of the most abundant wading birds in southeastern Brazil, and yet one of the least studied.They usually take two to three years to reach sexual maturity, breed in groups, and present sexual dimorphism (Morrison et al. 1978).Cormorants spend a considerable amount of time foraging either alone or in groups (Lekuona and Campos 1997) and are short-term divers.Certain wading birds are believed to damage aquaculture; however, their diet is barely known, except that it includes frogs, crabs, mollusks, aquatic insects, reptiles, and even small mammals, besides fish (Sick 1997).At the present study, we determined foraging efficiency of the Brazilian cormorant, Nannopterum brasilianus Gmelin, 1789, (Piacentini et al. 2015) and briefly discuss possible implications of food stealing by individuals of the same group.

MATERIAL AND METHODS
The study site was a roughly round artificial pond of approximately 0.84 ha (1 m deep) located at the University of São Paulo, Campus "Luiz de Queiroz", in Piracicaba, central-east region of the state of São Paulo, Brazil (22º43'S, 47º38'W)."Luiz de Queiroz" has 914,5 ha including fragments of native vegetation and agricultural fields, besides laboratories and office buildings.
The artificial pond where this study took place was constructed with cement in the late 1940s.The following species are known from this poind: Cyprinus carpio Linnaeus, 1758, Oreochromis niloticus (Linnaeus, 1758), and Pimelodus sp., all of which have been introduced by humans.The pond has no macrophytes and is surrounded by grass and a few trees.Domestic geese, Anser anser var.domesticus (Linnaeus, 1758); wild ducks, Cairina moschata Linnaeus, 1758); ireres, Dendrocygna viduata (Linnaeus, 1766); great white egrets, Ardea alba Linnaeus, 1758; and the snowy egrets, Egretta thula (Molina, 1782) are also present.People use the area around the pond as a city park.
The cormorant group was observed during a total period of 10h:12 min, early in the morning (7-10 am) and late in the afternoon (4-6 pm), for five days, in November 2000.Group size was determined on every observation period.Foraging behavior was observed with a 10 × 25 binocular by ad libitum sampling, and every occurrence of the behaviors we focused on was recorded (Altmann 1974, Martin and Bateson 1993, Lehner 1996).The following behaviors were considered: diving, fishing, and food stealing.
Diving lasting periods (in seconds) were recorded with a digital chronometer.Fish captured by cormorants could be recorded as the bird emerged to swallow the prey (Sick 1997).We considered a behavior as stealing or as an stealing attempt when an individual moved toward another and took, or tried to take, fish from it.Fishing success was calculated as the number of times a cormorant emerged with a fish, divided by the total number of dives.Stealing success was calculated by the number of times any cormorant was successful in taking another birds' fish divided by the total number of successful fishing attempts.
We used descriptive statistics on diving period, foraging success and stealing success.In addition, we used one-way Analysis of Variance (ANOVA) to test the possible relationships between diving lasting period and foraging success, stealing attempts and stealing success.

DISCUSSION
The foraging success of the Brazilian cormorant in the present study can be considered low when compared with the foraging success of the great white egret (Wiggins 1991).The great white egret employs a different foraging strategy, usually waiting for the prey in shallow waters.Such strategy can be individually more effective, but it is possible that it does not work when population densities are high or in large social groups (Crawley and Krebs 1992), as it is the case with the cormorant, even outside of the reproductive period.However, the anhinga, Anhinga anhinga (Linnaeus, 1766), has a foraging strategy similar to the Brazilian cormorant (Sick 1997, Carvalho 2010).
Although the foraging behavior of cormorants generally involves diving, these birds do not seem to be adapted to long periods of submersion (average at the present study = 10.41 ± 4.82 sec).As a matter of fact, shorter dives were significantly more associated with fishing success than longer dives in our data.This pattern suggests that the prey is possibly detected when the cormorant is still swimming, not diving.Dive would be the final attack over an already detected prey.Otherwise, if dives were exploratory, we would expect that longer dives would result in more prey catching success.However, foraging success by waterfowl can be influenced by environmental factors such as water depth, substrate and prey size.As a matter of fact, Brazilian cormorants can dive as deep as 20 m, what would imply on a distinct foraging strategy (Duffy et al. 1986, Wilson and Wilson 1988, Monteiro-Filho 1992, Carbone and Houston 1994, Sapoznikow and Quintana 2003).Therefore, our data pertains mostly to shallow waters.
Intraspecific competition for food can result in an increase in the time spent in foraging and greater risks associated with it (Alcock 1993).The apparent correlation between fishing and stealing behavior at the present study (see Fig. 2) corroborates this hypothesis, although some overlap would be expected.The stealing successful rate seems low (2.44%).However, the relative successful stealing rate is considerably higher (52.63%).This means that, although relatively rare, at least in small groups such as the one observed in the present study, stealing can be an efficient way to get food.In theory, stealing attempts would increase as group size increases.Further test of this hypothesis should be prioritized.
Although foraging success is related to how long the diving lasts, stealing is not.This pattern suggests that stealing is an opportunistic behavior.When individuals forage in groups, cooperatively or not, as soon as a bird gets a prey, another bird  In similar conditions to the present study (i.e., anthropic shallow water bodies with relatively small group sizes), the following inferences about the Brazilian cormorant's foraging behavior are made: 1) Brazilian cormorants are relatively efficient browsers and short-term divers; 2) Foraging success is related to dive lasting period, but stealing is not; 3) Stealing occurs at relatively low rates but tends to be an efficient way to get food.

Figure 1 .
Figure 1.Frequency of successful and unsuccessful dive durations.

Figure 2 .
Figure 2. Relationship between dive duration and stealing success.