Impaling in True Shrikes (Laniidae): a Behavioral and Ontogenetic Perspective

Behavioural Processes 69 (2005) 363–367

Impaling in true shrikes (Laniidae): A behavioral and ontogenetic perspective

Reuven Yosef a,∗, Berry Pinshow b

a International Birding and Research Centre in Eilat, P.O. Box 774, 88000 Eilat, Israel b Mitrani Department of Desert Ecology, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 84993 Midreshet Ben-Gurion, Israel Received 11 September 2004; received in revised form 14 February 2005; accepted 14 February 2005

Abstract

The impaling of prey is a behavioral trait restricted to the true shrikes (Laniidae). Here, we suggest the ontogeny of this behavior. We believe impaling originated from wedging behavior that occurs among several other groups of birds, including corvids. Accidental impaling during wedging was likely the behavioral precursor of purposeful impaling. Fidelity to impaling sites lead to the creation of caches, which were eventually used by females for male evaluation. Caching allowed males to increase their ﬁtness by using the caches as a display to attract potential mates. Further, caching is used by shrikes to demarcate territories, store food for inclement weather or periods of stress in the breeding cycle, divide labor between the breeding pair, and for “aging” while deterrent chemicals in prey decompose. © 2005 Elsevier B.V. All rights reserved.

Keywords: Laniidae; True shrikes; Impaling; Caching; Ontogeny; Evolution; Territoriality; Diet; Feeding behavior; Courtship

The role of impaling behavior in the biology of the Busbee, 1976). Other taxa have behaviors similar to true shrikes (Laniidae) has been extensively studied impaling. For example, some Australian Butcherbirds (e.g., Brewster, 1894; Watson, 1910; Donovan, 1929; (Craticidae spp.; Pizzey and Knight, 1997) and African Miller, 1937; St. Paul and Gwinner, 1967; Beven and Boubou Shrikes (Laniarius ferrugineus; Sonnenschein England, 1969; Wemmer, 1969; Yosef and Pinshow, and Reyer, 1984) are known to wedge prey, apparently 1988; Esely and Bollinger, 2003) and other animals to save handling time, however, these species never im- (e.g., Young et al., 2004). However, the evolution- pale prey on thorns. By contrast, in the Laniidae, verte- ary development of this unique tool is unstudied al- brate prey is impaled on sharp objects, decapitated and, though its ontogeny in young shrikes is well known in most cases, the brain consumed before other body (Miller, 1931; Wemmer, 1969; Smith, 1972, 1973; parts (Yosef, unpublished data). Impaling is deﬁned as the skewering of prey on a ∗ Corresponding author. Tel.: +972 3671290; fax: +972 86335319. sharp projection; “wedging” is the placing of the item E-mail address: [email protected] (R. Yosef). in the fork of a substrate (branch, barbed wire, etc.)

0376-6357/$ – see front matter © 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2005.02.023 364 R. Yosef, B. Pinshow / Behavioural Processes 69 (2005) 363–367 that allows the predator to manipulate and feed on a food (Yosef and Pinshow, 1989; Sarkozi and Brooks, prey item. In some cases, while the predator attempts 2003). During the period of prenuptial display, male to wedge the prey it may be accidentally impaled on shrikes were observed to impale inedible objects such a sharp projection, but intentional and systematic im- as rags, snail and eggshells, fæcal sacs or even bread paling, as it occurs in the true shrikes has not been crusts, ostensibly to boost the visual effect of the cache documented in any non-Laniidaen bird species. Both (Durango, 1956; Lorenz and St. Paul, 1968; Yosef and wedging and impaling are considered tools that facili- Pinshow, 1988; Leonard, 1992). In this light, it was tate dismemberment of prey at lower energetic costs to suggested that male quality was evaluated, not only by the predator (Schon, 1994; Cade, 1995). the visual impression of the conspicuous cache, but also Most studies of impaling have concentrated on by the composition of the impaled prey items; this even the Loggerhead (Lanius ludovicianus), Red-backed (L. though caches were continuously subject to kleptopara- collurio), Woodchat (L. senator) and Great Grey Shrike sitism (Yosef, 1989). In addition, fitness was positively (L. excubitor). Field observations confirm that the abil- correlated to initial cache size. Not only was repro- ity to impale prey develops in the young of these ductive success higher in males with larger caches, but species in the first 4–5 weeks after fledging (Miller, also polygynous breeding occurred in them more often 1931; Cade, 1967; Wemmer, 1969; Smith, 1973; Bus- (Yosef and Pinshow, 1988; Yosef et al., 1991). bee, 1976; Yosef, unpublished data). Although Lorenz Esely and Bollinger (2003) found a positive correla- and St. Paul (1968) concluded that impaling was innate tion between impaled prey abundance and the number in young shrikes, they suggested that it could only be of fledglings produced per successful nest. The facts mastered by practice and experience. Busbee (1976) that shrikes persist in maintaining conspicuous caches also considered experience an important component in even when their young have hatched and that they im- the development of vertebrate predatory behavior and pale inedible objects such as egg shells and fæcal sacs concluded that a definite ontogeny must occur before under the continual threat of kleptoparasites, which impaling proficiency could be achieved. These ideas may even endanger their young, have prompted several are consistent with the findings of Ashmole and To- authors to suggest that this exhibitionism has a role in var (1968) and Recher and Recher (1969) showing that reducing the energetic costs of territorial defense dur- capture rate, capture efficiency, prey size and handling ing the most strenuous part of the birds annual life cycle time improved with age in avian predators indicating (Mizzel, 1993). In fact, Mizzel (1993) and Sarkozi and that there is a learning component in avian predatory Brooks (2003) hypothesized that impaling plays a role behavior. in advertisement of territory ownership and the territo- Shrikes are similar to diurnal raptors (Falconi- rial boundaries defended. formes) in their predatory behavior, but in contrast they Other explanations that have been proffered to ex- do not posses the strong talons that the larger raptors plain impaling behavior. For example, many studies on use to dismember prey (Schon, 1994; Cade, 1995; Van- foraging have suggested that caching or hoarding, i.e., der Wall, 1990). It has been suggested that shrikes have the creation of a larder for later use, is the major func- overcome this limitation by evolving impaling behav- tion of impaling (Karasawa, 1976, 1982; Carlson, 1985; ior that allows them to increase the size of exploitable Vander Wall, 1990; Severinghaus and Liang, 1995). food items (Whyte, 1887; Olsson, 1985; Yao, 1985). Burton (1999) proposed that the impaling of old nest Wemmer (1969) and Valera et al. (2001) found that material by shrikes for later use results in inedible ob- the unpredictable and transitory nature of food surplus jects remaining impaled after the construction of a new seemed crucial to initiate impaling behavior. Moreover, nest is accomplished. Burton suggested that this behav- the composition of caches of impaled food was found to ior could have been the progenitor of the impaling of be a function of the distribution and accessibility of the large prey items for dismemberment. Applegate (1977) prey (Whyte, 1887; Durango, 1956; Kobayashi, 1980; theorized that impaling might serve to clearly divide Yosef and Grubb, 1993; Tryjanowski et al., 2003). sex-specific tasks between the parents, i.e., males hunt Caches made prior to pair bonding and the start of and impale while the females feed themselves and their the breeding season may be indicative to females of young from the caches. Yosef and Whitman (1992) re- male quality and the potential parental ability to supply ported an interesting exaptation of impaling behavior. R. Yosef, B. Pinshow / Behavioural Processes 69 (2005) 363–367 365

Fig. 1. Ontogeny of impaling behavior in true shrikes, Laniidae.

They found that aposematically colored and chemically ing sites has carried over into their adult behavior. If defended lubber grasshoppers (Romalea guttata) were viewed in the perspective of evolutionary time, and tak- impaled by loggerhead shrikes, aged until the deterrent ing into account that no other avian species has ever chemicals decomposed, and eventually consumed. gone beyond the stage of dabbing or wedging (Smith, Consolidating at this juncture (Fig. 1), we posit that 1973), we consider the fidelity to favorite impaling sites impaling is an innate behavioral characteristic that is to be the basis for the evolution of this behavioral trait refined by learning and practice. Fledgling shrikes are which evolved from simple dabbing by fledglings, to known to play with inedible objects while still being wedging while gaining experience, and eventually to fed by their parents and to indulge in “dragging” behav- proficient impaling in adults that are now able to ex- ior that later develops into what was termed “dabbing” ploit prey that would otherwise be inaccessible. (Smith, 1972; aka “Tupfbewegungen”; Lorenz and St. Based on our observations in the Sede Boqer area, Paul, 1968). Once the fledglings are able to catch prey Israel (1986–1989), and at the MacArthur Agro- for themselves, they develop individual variations in ecology Research Centre, in Florida (1989–1993), we their prey handling. consider sexual selection by females to have been a The sole use of impaling by fledglings is to assist selective force behind the various exaptations of impal- in the dismemberment of prey. The young also return ing that have been reported. The pattern of change in to impale where they successfully impaled previously, impaling behavior might have gone like this: in the past usually at places where they engaged in dabbing (Yosef, when females arrived at the breeding grounds, they unpublished data). We think that this fidelity to impal- evaluated the male and his territory quality by visually 366 R. Yosef, B. Pinshow / Behavioural Processes 69 (2005) 363–367 identifying the locations of the cache sites and their fected as impaling is unique in nature and requires fur- contents. Responding to what the females were using as ther study to understand the ecological processes driv- an index of quality, the males probably not only resorted ing its development and diversification in the Laniidae. to killing prey beyond their own needs and impaling This is paper number 479 of the Mitrani Department the excess in their caches, but also to adding small prey of Desert Ecology. items that could otherwise be consumed with relatively little handling cost. In order to enhance the visual impression of the cache, the males also impaled inedible, but often colorful, objects. This is probably when References aposematically colored, chemically defended insects Applegate, R.D., 1977. Possible ecological role of food caches of the were impaled—initially as visual cues, but that after Loggerhead Shrike. Auk 94, 391–392. a time detoxified and became edible (Yosef and Whit- Ashmole, N.P., Tovar, H., 1968. 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