The kleptoparasitic and commensal association of Dalmatian Pelicans Pelecanus crispus with Great Cormorants Phalacrocorax carbo Kleptoparasitism och kommensalism mellan krushuvad pelikan Pelecanus crispus och storskarv Phalacrocorax carbo

5 Citation: Källander H. 2020. The kleptoparasitic and commensal association of Dalmatian Pelicans Pelecanus crispus with Great Cormorants Phalacrocorax carbo. Ornis Svecica 30: 5–12. https://doi.org/10.34080/os.v30.20265. Copyright: © 2020 the author(s). This is an open access article distributed under the CC BY 4.0 license, which allows unrestricted use and redistribution, provided that the original author(s) and source are credited. R E S E A RCH PA PE R


Introduction
Kleptoparasitism, the stealing of food from other individuals, has attracted much interest among ornithologists and many hundreds of papers on the topic exist. Several reviews have been devoted to this foraging behaviour (Brockmann & Barnard 1979, Furness 1987, Morand-Ferron et al. 2007, Iyengar 2008. Barnard & Thompson (1985) analysed in great detail the kleptoparasitic association between Black-headed Gulls Croico cephalus ridibundus on the one hand and Northern Lapwings Vanellus vanellus and European Golden Plovers Pluvialis apricaria on the other. Both intraspecific and interspecific kleptoparasitism is a common foraging method in both terrestrial and aquatic environments and may have negative effects on the host (Stienen et al. 2001) and positive effects on the parasite, e.g. by promoting nestling growth (García et al. 2013).
Commensalism, in which an individual benefits from associating with individuals of another species without having any negative impact on the latter's food intake is equally common and the literature is similarly extensive. In the terrestrial environment, it usually takes the form of 'flushing' or 'beating' by which insects and other arthropods become exposed because of the host's movements; in aquatic environments it usually means that food particles become available to the commensal because of the host's feeding activities. As examples one could mention Little Grebes Tachybaptus ruficollis that associate with dabbling ducks (Siegfried 1971, Robson 1975 or various waterbirds that associate with swans Cygnus spp. (Bailley & Batt 1974, Beven 1980, Merilä & Ohtonen 1987, Källander 2005, Dijksen & Ouweneel 2005, Gyimesi et al. 2012. Byrkjedal et al. (1997) described how Velvet Scoters Melanitta fusca that were digging for echinoderms in a sandy substrate thereby disturbed large numbers of polychaete worms that were exploited by Red-necked Grebes Podiceps grise gena. Another interesting association is that between neotropical otters Lontra longicaudus which drove fish in front of them so that various species of piscivorous birds got access to the fish (D'Angelo & Sazima 2014). In the marine habitat, a variety of birds associate with whales and dolphins (reviewed by Evans 1982;Hodges & Woehler 1995, Camphuysen & Webb 1999, Orgeira 2004, Anderson & Lovvorn 2008, Hebshi et al. 2008, Rossi-Santos & Flores 2009, Rudd et al. 2011. Fish are often relatively large (especially in relation to the size of a bird's bill) and take long to swallow, which make both intraspecific and interspecific klepto parasitism a common foraging method among pisci vores. In the present contribution the kleptoparasitic and commensal association of Dalmatian Pelicans Pelecanus crispus with Great Cormorants Phalacrocorax carbo is described.

Study areas
Observations were carried out at Megali Prespa in north-western Greece mainly in June and early July in 1991, 1993, 1995and in May 2015and 2018, at the Karla reservoir in central Greece in January 2016 and at Kerkini reservoir and the river Strymonas in northern Greece in March 2013 and May 2018. Megali Prespa is a deep lake (maximum 54 m) with clear water, shared between Greece, Albania and North Macedonia. It is surrounded by mountains but nearer to its southern end it is shallower. The pelicans nest in Mikri Prespa but nearly all of their feeding takes place in Megali Prespa and the same is true for cormorants. So, every day they have to fly across the c. 1 km wide isthmus that separates the two lakes. They often fly far out on the 176 km 2 large lake and in recent years much feeding has taken place near the large island of Golem Grad in North Macedonia.
At Kerkini, the situation differs considerably from that at Prespa. Kerkini was created in 1932 by the building of a large dam across the river Strymonas. First of all, the water is much less clear and the cormorants breed at considerably larger colonies than at Prespa. Thus, in 2013, 5,600 cormorants were breeding at Kerkini. Even though cormorant numbers have since decreased to about 4,500 (T Naziridis pers. comm.), fishing flocks regularly contained more than a thousand cormorants on the lake and several hundred on the River Strymonas.
Karla was a natural lake that was partly drained from 1962 to 1965. Later (in the 1990s to 2000s) a large reservoir (mainly for irrigation purposes but also for wildlife) was built around part of the former lake bed. The lake's maximum depth is less than two metres. Part of it is surrounded by dykes constructed from rocks and stones. The surrounding lowland is crossed by drainage canals. The lake's water level is regulated and neck erect and held slightly forward, the bill pointing obliquely downwards, then this acted as a strong cue to both other cormorants and other pelicans, so within seconds a small group gathered around the first pelican. The number of cormorants was usually rather low (the median value being 6). In just one instance their number reached 190 and this situation also differed in that pelicans seemed to engage to a great deal in kleptoparasitism.
Cormorants nearly always dived instantly on landing. Sometimes a pelican threatened another pelican and drove it away from the cormorant group. Fishing sessions were usually of short duration lasting a mean of only 114 s. Either the pelican or the cormorants then flew off, often to another actively fishing group. The hovering low over the surface by Yellow-legged Gulls Larus michahellis also made pelicans fly to the site.
Out of 274 recorded 'strikes' , pelicans swallowed a fish on 146 (53.3 %). Most of these instances were no doubt commensal, i.e. the pelicans got fish that had tried to escape from the cormorants by swimming upwards towards the surface. Indeed, from a high vantage point west of the lake it was on several occasions possible to see the shoals just below the surface close to the place where a cormorant had surfaced. In contrast, the attacks by the pelican rather seemed to make the shoals return into deeper water which may explain the short duration of the fishing bouts.
Kleptoparasitism was established c. 40 times with attacks where the pelican succeeded in securing the fish on nine occasions (c. 18 %). Once a big fish was lost into the water by both the cormorant and the pelican. However, the number of times that kleptoparasitism could be established with certainty was probably underestimated, because on many occasions a pelican stroke close to a surfacing cormorant and the pelican swallowed while the cormorant surfaced without a fish. From the high hills to the west of the lake one could see through the clear water of Megali Prespa how pelicans followed a diving cormorant, changing direction as the cormorant did so. Those kleptoparasitic attacks where a pelican got the fish involved relatively large fish.

KERKINI
At Kerkini, the situation differed considerably from that at Prespa. The large flocks of cormorants were almost always accompanied by numerous Dalmatian Pelicans the lake contains a lot of fish. Its fish fauna is dominated by cyprinids. It also holds one of six Greek breeding sites for Dalmatian Pelicans and three for Great White Pelicans Pelecanus onocrotalus.

Methods
Pelicans were observed from the lake shores and the banks of the reservoirs with the aid of telescopes (Kowa TSN with a 20× ocular during 1991-1995 and with a Carl Zeiss diascope 85 TL with a 20-60× zoom in all later years). During the first years, observations were talked into a small tape recorder and later transcribed; in later years the material was entered directly into note books. At Prespa the focus was on the association between pelicans and cormorants whether kleptoparasitic or commensal. For this reason, the duration of the feeding associations was measured and the number of the two species recorded. At the two other sites, the studies were concentrated on kleptoparasitism although commensalism was also observed. At all three sites the kleptoparasitism was recorded as number of attacks on the cormorants that were successful, i.e. resulted in the pelican stealing the fish from the cormorant. Commensalism was much more difficult to record and therefore no hard data on its occurrence could be obtained. However, the number of 'strikes' seen at Megali Prespa and reported below probably largely represent cases of commensalism. It should be emphasized that observation distances were often long, about a hundred meters at the Strymonas river and often many hundred metres elsewhere.

MEGALI PRESPA
At Megali Prespa the association between pelicans (both Dalmatian and Great White Pelicans) appeared to be mutual: pelicans were attracted to cormorants and benefited from fish that the cormorants made available by their deep-diving fishing method, while cormorants seemed to use the behaviour of the pelicans to locate fish shoals. Pelicans were most often foraging singly or in small groups of just a few individuals (mean = 3.2, SD = 2.08, n = 124). When a pelican rushed or flew towards a cormorant in a very typical posture with  which were spread out among the cormorants ( Figure  1). The pelicans followed the cormorants as they swam or flew to a new position on the lake. When a cormorant captured a fish, a pelican would immediately make a short flight towards it which usually made other pelicans join in and often there was much movement and excitement ( Figure 2). This, together with often long observation distances often made it difficult to determine the outcome of the attacks with certainty. However, it was usually possible to see the pelican's typical swallowing movements. Overall, pelicans were successful in c. 19 % of their attacks on cormorants at Kerkini.
A smaller material was obtained from the River Strymonas, where the interactions between cormorants and pelicans could be studied at closer range. In early summer, cormorants fly and swim upstream the river in large numbers and are followed by White Storks Cico nia ciconia, Black Storks C. nigra, Eurasian Spoonbills Platalea leucorodia, Grey Herons Ardea cinerea, Little Egrets Egretta garzetta and Yellow-legged Gulls, all of which try to use the cormorants commensally by following the river banks and shifting to the bank closest to the cormorants. Pelicans also followed the cormorants and kleptoparasitized them. In 2018, 4 out of 13 'strikes' by Dalmatian Pelicans towards pelicans were successful (31 %). However, if one includes the number of flights towards cormorants that were not followed by a strike, i.e. when the pelican interrupted its attack at an early stage, their success rate was very much lower.
Pelicans also took advantage of the cormorants as they drove small fish towards the shore or into vegetation. Many positive strikes were seen in such situations (commensalism). How successful the pelicans were at obtaining fish by commensalism unfortunately could not, however, be determined. Flocks of Black-headed Gulls, which plunge-dived for small fish, often also accompanied the cormorants. As an example, more than 20 such positive dives by gulls were recorded over a flock of cormorants that followed small fish into a shallow area.

KARLA RESERVOIR
As at Kerkini, pelicans associated closely with flocks of cormorants and often flew together with them to the place where the cormorants landed. Pelicans attacked cormorants that surfaced with a fish and, as at Kerkini, an attack by a pelican always made other pelicans head for the same cormorant. Out of 184 attacks recorded 41 (22.3 %) were successful (I did not record attacks that were not followed by a strike). In these cases, fish were relatively large. As at Prespa, cormorants and pelicans reacted to Yellow-legged Gulls that hovered low over the surface and quickly flew to the spot. A similar observation was made by Jönsson (1984) who studied groups of European Shags Phalacrocorax aris totelis that were fishing off the island of Skopelos in the northern Sporades. The Shags were kleptoparasitized by Yellow-legged Gulls. When the Shags ceased fishing, the gulls started searching for fish shoals on their own. When one was found, their hovering and calling immediately recruited the Shags which began exploiting the shoal and were again kleptoparasitized by the gulls.

SOME GENERAL OBSERVATIONS
Overall some 20 % of kleptoparasitic attacks resulted in the pelican obtaining the fish. Twice a pelican was seen trying to obtain a fish from a cormorant in flight but with no success. Cormorants made no attempts at avoiding being kleptoparasitized. Only a couple of times they were seen threatening or trying to bite a pelican. In fact, at Prespa cormorants reacted to a striking pelican by flying to it and immediately diving under it.
At Kerkini, Dalmatian Pelicans were also seen associating with flock-fishing Pygmy Cormorants Micro carbo pygmaeus. About 200 Pygmy Cormorants were fishing in a shallow, vegetated bay and were followed by some ten pelicans. Probably the cormorants' activities made fish available to the pelicans but one instance of a (successful) kleptoparasitic attack was also recorded. Several attempts at intraspecific kleptoparasitism among pelicans were also observed, but only two were successful.

Discussion
The association between Dalmatian Pelicans and Great Cormorants appear to be a very close one. The observations at Prespa suggest that at this lake the association may benefit both parties: the pelicans by increasing their intake of fish (Crivelli & Visi 1981, Maximidi et al. unpublished data) and the cormorants by finding fish shoals with the aid of pelicans. Although kleptoparasitism was very common at the two other sites, commensalism also occurred quite commonly.
Even if there is a cost to the cormorants in the form of fish lost to kleptoparasitic pelicans, the cormorants seem to have no possibility to avoid this cost. However, as the number of cormorants always was much larger than the number of pelicans, the individual loss no doubt was negligible especially at the two sites (Kerkini and Karla) where cormorants formed huge fishing flocks. Intraspecific kleptoparasitism between cormorants, which was relatively common, was probably more costly for the cormorants than was that of the peli cans' but the formation of large fishing assemblies by cormorants likely increases capture efficiency enough to greatly outweigh this cost (Källander 2013).
The attacks on cormorants were often very fierce and on a total of 31 occasions (all three study sites together) a pelican was seen holding the cormorant until it dropped its fish (only once a cormorant managed to keep it). To use an anthropomorphic term, the way that pelicans handled the cormorants was rather cruel. They held them across their necks and heads and once across the body and once in the wing, the cormorant struggling to get loose. This violent treatment of the cormorants has also been seen at Lake Joaninna in western Greece (Catsadorakis 2002).
It seems that the association between pelicans and cormorants is a very common and wide-spread phenomenon. Apart from the localities studied here, it has also been mentioned by Romashova (1994) from the Volga delta and P-E Jönsson (pers. comm.) also saw the close association between Dalmatian Pelicans and cormorants in the Donau delta.
Kleptoparasitism has also been observed in the American White Pelican Pelecanus erythrorhynchos (O'Malley & Evans 1983, Anderson 1991. In both the cited studies, these attacks were directed at flocks of Double-crested Cormorants Phalacrocorax auritus. In the former study only two out of ten attacks were successful while 26 of 52 attacks (33.3 %) were so in the latter. These figures agree rather well with those obtained in the present study, which seems to be the first one to quantify kleptoparasitism as a feeding method in the largest species of pelican, the Dalmatian Pelican.
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