Frugivory in Raptors: New Observations from Australia and a Global Review

Simple Summary: Raptors (birds of prey) typically consume vertebrate and invertebrate prey. However, some species have also been recorded consuming fruits. We described instances of the Black Kite ( Milvus migrans ) and Whistling Kite ( Haliastur sphenurus ) consuming avocado ( Persea americana ) fruit in northern Australia. This appears to be the ﬁrst instance of fruit consumption by raptors in Australia. We also review and document instances of fruit consumption by 29 species of raptors across the world, signiﬁcantly more than previous reviews. Abstract: The diets of raptors are some of the best studied and well-known of all bird groups. Raptors are typically carnivores, hunting and feeding on vertebrates and, for some species, invertebrates. Here, we described instances of the Black Kite ( Milvus migrans ) and Whistling Kite ( Haliastur sphenurus ) consuming non-native avocado ( Persea americana ) fruit in commercial orchards in northern Australia, over multiple years. This appears to be the ﬁrst instance of frugivory by raptors in Australia. We review instances of frugivory for other raptor species globally. This review ﬁnds that 29 species of raptor from the families Falconidae, Accipitridae and Cathartidae have been recorded consuming fruit, signiﬁcantly more than previous reviews.

However, major reviews of Australian raptors [9][10][11][12][13] and other peer-reviewed and grey literature have not noted frugivory from raptor species occurring on that continent. Here, we described instances of frugivory in the Black Kite (Milvus migrans) and Whistling Kite (Haliastur sphenurus) in northern Australia over multiple years and review instances of frugivory for other raptor species globally. We define frugivory as the consumption of fruit, in line with other reviews [5,14], but do not imply raptors conduct exclusive or extensive frugivory (e.g., [15]).

Observations
In 2002, Jack Leighton (JL) first observed Black Kites around avocado (Persea americana) orchards (a tree species native to Mexico, but widely planted in commercial crops in many Birds 2021, 2 340 move to the east as their breeding grounds dry out (JL pers. obs.), although movement patterns of Black Kites in Australia are not well known [9]. Most birds observed feeding on avocados were adults.
Avocado growers do not seem to have a concern with this scavenging behaviour, as the decaying fruit would otherwise harbour fungi. In nineteen years since the initial observations, no Black Kites have been observed picking or consuming fruit directly from the trees.

Literature Review
We reviewed major Australian and international handbooks, conducted literature searches using Google, Google Scholar and Scopus (with search terms which included the words "raptors" or "birds of prey", with "frugivory" or "fruit" or "frugivorous") and reviewed individual raptor species profiles in online databases such as Birds of the World (https://birdsoftheworld.org/, accessed on March-July 2021) in March-July 2021 for instances of frugivory in raptors. Searches were conducted in English, but non-English language sources were interrogated if they turned up in searches. Where relevant sources were found we interrogated the references in those sources and searched for other papers that may have cited those sources. All material that had original details of frugivory in We did not record quantitative data on fruit biomass ingested per unit of time, nor the relative intake of fruit compared to other prey types. JL has not observed Black or Whistling Kites breeding on the Atherton Tablelands. Their breeding usually occurs west of the Great Dividing Range when the seasons are good (i.e., rodent or locust plagues) and move to the east as their breeding grounds dry out (JL pers. obs.), although movement patterns of Black Kites in Australia are not well known [9]. Most birds observed feeding on avocados were adults.
Avocado growers do not seem to have a concern with this scavenging behaviour, as the decaying fruit would otherwise harbour fungi. In nineteen years since the initial observations, no Black Kites have been observed picking or consuming fruit directly from the trees.

Literature Review
We reviewed major Australian and international handbooks, conducted literature searches using Google, Google Scholar and Scopus (with search terms which included the words "raptors" or "birds of prey", with "frugivory" or "fruit" or "frugivorous") and reviewed individual raptor species profiles in online databases such as Birds of the World (https://birdsoftheworld.org/, accessed on March-July 2021) in March-July 2021 for instances of frugivory in raptors. Searches were conducted in English, but non-English language sources were interrogated if they turned up in searches. Where relevant sources were found we interrogated the references in those sources and searched for other papers that may have cited those sources. All material that had original details of frugivory in raptors were included (books, book chapters, peer-reviewed journal articles, non-peerreviewed articles, theses, websites, databases).

Results of Literature Review and Discussion
The Whistling Kite takes a variety of small animals (but particularly introduced European Rabbits Oryctolagus cuniculus and European Hares Lepus europaeus occidentalis) and carrion (especially in winter, the non-breeding season), including mammals, birds, reptiles, fish, crustaceans, insects, large carcasses, and offal [9]. In Australia, the Black Kite is a scavenger, taking carrion, offal and garbage, but also taking small mammals, small birds, reptiles, frogs, grasshoppers and fish [9]. It can exploit plagues of mammals (e.g., European Rabbits, House Mouse (Mus musculus) and Long-haired Rats) and locusts and grasshoppers [9].
The observations of Black Kites and Whistling Kites consuming avocado fruit over multiple years appear to be the first instances of frugivory by wild raptors in Australia. This represents the first instance of frugivory for the Whistling Kite, an endemic species to Australia, New Guinea, the Solomons and New Caledonia [9]. For the Black Kite, a raptor with a range from Africa, Europe, Asia and Australia, there are few other records of frugivory, none from the Australasian subspecies M. m. affinis and none of consumption of avocado. Those records include Thiollay [3] (p. 67), who stated that breeding Black Kites in the savannas of central Ivory Coast in Africa included a high proportion of oil palm Elaeis guineensis fruits in its diet and "even brought them in large numbers to their nest to feed the young, a remarkable practice, given that it would seem energetically unprofitable to carry in such largely indigestible fruits, one by one". Cramp and Simmons [20] noted the only plant food recorded for Black Kites was the pericarp of oil palm nuts, while no records of fruit consumption by this species have been recorded in Asia [21,22] nor Australia [9].
In a review of frugivory by vertebrates in the adjoining Oriental (Indomalayan) Region, Corlett ([21], p. 430), suggested "hawks and their relatives generally feed on vertebrates and large insects, but there are reliable records of the consumption of small fruits by the Pacific Baza, Aviceda subcristata (Bell 1984 [23], Debus 1994 [24]), and Roberts (1991) [25] states that 'other authors' (not named) have recorded frugivory by the Oriental Honeybuzzard, Pernis ptilorhynchus". Despite the breeding range for Pacific Baza extending from Australia, Indonesia, Papua New Guinea, and Solomon Islands, it appears all records of frugivory are from New Guinea (Table 1).
Major monographs on raptors or birds more generally and three previous reviews on frugivory in raptors (or specific families of raptors) identified different numbers and species (Table 1). Brown and Amadon [26] and Ferguson-Lees and Christie [2] in their reviews of raptors of the world identified fruit consumption by 13 and 18 species of raptors, respec-Birds 2021, 2 343 tively, but while they provided a list of references for each species, did not cite the original sources of frugivory. Galetti and Guimarães [5] in describing seed dispersal by Crested Caracaras (Caracara plancus) identified 13 raptor species that consumed fruit, largely drawn from the 1995 Handbook of the Birds of the World ( [27]; and chapters within, i.e., [1,3,4]) as well as source material used in that Handbook and subsequent records until 2004, but did not cite Ferguson-Lees and Christie [2]. Shlee [6], in documenting the first instance of the King Vulture (Sarcoramphus papa) consuming fruit (moriche palm Mauritia flexuosa), identified eight raptor species that consumed fruit, but did not cite del Hoyo et al. [27], Ferguson-Lees and Christie [2], or Galetti and Guimarães [5]. Pérez-Méndez and Rodríguez ( [14], p. 141), in their review of raptors as seed dispersers, suggested "Sixteen of the 312 raptors considered by Ferguson-Lees and Christie [2] consume deliberately fruits at least occasionally", listing those identified by Ferguson-Lees and Christie [2] (although they seem to have missed the Long-crested Eagle (Lophaetus occipitalis) and Great Black Hawk (Buteogallus urubitinga), which were both identified by Ferguson-Lees and Christie [2]), but they list 20 in total from that source, Galetti and Guimarães [5] and others. The online Birds of the World database, which was largely drawn from Handbook of the Birds of the World entries ( [1,3,4], and individual species accounts within, plus additional information since 1994), as well as from Ferguson-Lees and Christie [2], documented 25 species as consuming fruit as of July 2021, but did not include records of the Oriental Honey-buzzard, Great Black Hawk and Plumbeous Kite (Ictinia plumbea) ( Table 1). Based on these reviews, plus the addition of the Whistling Kite from the observations described in this paper, there are 29 species that have been known to consume fruit or other vegetable matter globally (Table 1). In addition, Ospreys (Pandion haliaetus) have been observed deliberately ingesting green algae (Rhizoclonium sp., belonging to the family Cladophoraceae) and slime near the banks of an agricultural water reservoir at Tenerife, Canary Islands [28].
The majority of the raptor species recorded consuming fruit, and also the most frequently consumed fruits, are rich in lipids (genera Elaeis, Raphia, Cocos, Spondias, etc.) [14]. Galetti and Guimarães [5] suggest that lipid-rich fruits could be used by generalist or insect-specialized raptors because they are chemically analogous to animal prey and may satisfy the raptor's lipid needs. Likewise, Shlee [6], in observing King Vultures consuming fruits of moriche palms Mauritia flexuosa in Venezuela, suggested the fat content of that fruit may partially compensate for a lack of carrion.
Avocado fruits also have a high lipid content [29], which increase as they ripen [30]. Besides the observation of the Black Kite and Whistling Kite in this paper, the Black Vulture (Coragyps atratus) is the only other raptor species known to consume avocados (Table 1). Röhl [31] found that American Black Vultures feed on avocado when carrion is scarce.
The year 2002 was a bad drought year in North Queensland [32], and there were noticeably lower numbers of grasshoppers and locusts, which would be an important food source for Black Kites and Whistling Kites, other than mice and native rats (JL pers. obs.), and so may also have been a driver for avocado fruit consumption by these species. Similar to our observations on the Atherton Tableland, Woods [33] (p. 237) suggested many (non-raptor) bird species "are fond of ripe, soft avocados" in California, USA, and suggested that as the fruits are picked when hard, there is little conflict. The ripe (and thus soft) nature of the avocado fruit consumed by Black and Whistling Kites outlined in our observations also corresponds with frugivorous behaviour of other raptors, e.g., "rotting coconuts" [34], "rotten pumpkins" [35] and "rotting apples" [2].
However, at least nine raptor species consumed berries, figs and apples (including some species that have only been recorded consuming these), which would have lower lipid content than the fruits described above. The review by Shanahan et al. [36] of figeating vertebrate fauna did not include any raptors, despite three species being identified in our review.
Small green fruits: [5,43] "There is an unconfirmed record of this species taking small green fruits [5]". [109] Source of 'P. Madrigal, pers. comm' in Galetti and Guimarães [5] is Garrigues [110] * Largely drawn from Handbook of the Birds of the World entries ( [1,3,4] and individual species accounts within, plus additional information since 1994). Accessed on 12 July 2021.ˆthis food source is not listed in a review of birds consuming fungi [111].

Conclusions
Here, we document the first instances of frugivory by wild raptors in Australia, including the first instance frugivory for the Whistling Kite and the first instance of the Black Kite consuming avocados. Considering the lack of records in Australia, it is likely that the frugivory for both species is opportunistic, exploiting locally abundant fruit when other resources are scarce. Nonetheless, observations of Black Kites feeding on fallen avocado fruits over a period of almost 20 years suggests a more regular consumption, in North Queensland at least. In addition, we found 29 species of diurnal raptors documented in the literature (and our observations) to have consumed fruit, up from the 13 in the review by Galetti and Guimarães [5] and 18 by Ferguson-Lees and Christie [2]. The findings here support the statement by Galetti and Guimarães [5] (p. 134) that "Based on the scarcity of natural history data for several forest-dwelling species, it is possible that more species of kites and hawks eventually consume fruits, acting as non-specialized frugivores". However, we suggest it is likely that more raptor species than those that are forest-dwelling are likely to consume fruit. The episodic nature of the activity for most species may contribute to scarcity of records. Further observations of frugivory by raptors should be documented in order to better understand the frequency of the behaviour.

Data Availability Statement:
The new data were created in this study are available on request.