Interspecific Territorial Behavior of Two MourningCloaks (Nymphalis antiopa) in Response to a DiurnallyActive Big Brown Bat (Eptesicus fuscus)

Authors: Anich, Nicholas M., White, J. Paul, and Anich, Stephen E.

Source: Northeastern Naturalist, 27(3)

Published By: Eagle Hill InstituteURL: https://doi.org/10.1656/045.027.0308

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Interspecific Territorial Behavior of Two Mourning Cloaks (Nymphalis antiopa) in Response to a Diurnally Active Big Brown Bat (Eptesicus fuscus) Nicholas M. Anich1,*, J. Paul White2, and Stephen E. Anich3

Abstract - Nymphalis antiopa (Mourning Cloak), a common daytime-flying butterfly, is known to ex-hibit territorial defense against small animals that share the same airspace. However, a bat seems to be an unlikely target for this aggression because bats are potential predators and diurnal bat activity is rarely observed. Here, we report territorial behavior of 2 Mourning Cloaks in response to a diurnally active Eptesicus fuscus (Big Brown Bat). This report is unusual in that it involves a non-predatory cross-phylum interaction, between an insect and a mammal.

Introduction. Territorial boundaries can be delineated by sound (Liu and Kroodsma 2007), physical actions (Noble 1939), or scent (Smith et al. 1989) to mark focal elements within a home range and are defended against conspecifics (Noble 1939) and sometimes heterospecifics (Jones et al. 1998, Schultz and Switzer 2001). Male Nymphalis antiopa (L.) (Mourning Cloak) butterflies hold territories by perching at different locations around their territories and flying short patrols to search for potential mates and intruders (Bitzer and Shaw 1983). When a conspecific is encountered, the male pursues to either drive the butterfly from its territory if it is another male or copulate with it if it is a female—typical behavior for temperate-zone butterflies (Benson et al. 1989, Bitzer and Shaw 1983). This pursuit behavior can be vigorous, and Mourning Cloaks may have difficulty identifying moving objects at a distance, resulting in frequent pursuits of birds and even falling leaves if they fall at speeds similar to butterfly movement (Bitzer and Shaw 1983). Daytime bat activity can be attributed to disease (Bernard and McCracken 2017), roost disturbance (Sparks et al. 2003), heat stress (Bartonička and Řehák 2007), mating (Boyles et al. 2006), water consumption or foraging (Speakman and Racey 1989), practice flights by juvenile bats (Davis and Hitchcock 1965; Kunz 1973, 1974) and abrupt ambient temperature increases (Downs et al. 2015, Edson et al. 2015, Speakman 1990). The cave-hibernating Eptesicus fuscus (Palisot de Beauvois) (Big Brown Bat) is found throughout the Great Lakes region and, like most species, this bat is deterred from flight by heavy rain or air temperatures below 10 °C (Kurta 2017). In the spring months of March–May, when such conditions are prevalent at night, daytime flights of Big Brown Bats have been documented in Wisconsin by multiple observers (Natural Heritage Inventory Program, Wisconsin De-partment of Natural Resources, Madison, WI, unpubl. data). Observation. The observation reported here took place near a seasonal residence on Lake O’Brien (46°17'48"N, 90°24'14"W), in the Township of Knight, 7.8 km south of Upson in Iron County, WI. On 3 May 2019, S.E. Anich observed 5 bats (species not determined) flying during the day. At ~1500 hours CDT, he observed a Mourning Cloak persistently following an active Big Brown Bat (Fig. 1). The bat was flying back and forth repeatedly over an area of driveway, a warm microclimate on the cool spring day. One butterfly closely followed every maneuver of the bat during the entirety of the event

1Wisconsin Department of Natural Resources, 2501 Golf Course Road, Ashland, WI 54806. 2Wiscon-sin Department of Natural Resources, Madison WI 53703. 312601 Yukon Trail, Minocqua, WI 54548. *Corresponding author - nicholas.anich@wisconsin.gov.

Manuscript Editor: John Rawlins

Notes of the Northeastern Naturalist, Issue 27/3, 2020

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which lasted 5 minutes, and a second butterfly joined in the pursuit for ~1 minute towards the end of the observation period, perhaps as the bat flew into a second butterfly territory, or perhaps the second butterfly was pursuing the first butterfly (Fig. 2). Photographs were

Figure 1. A Nymphalis antiopa (Mourning Cloak) pursuing an Eptesicus fuscus (Big Brown Bat) near Upson, Iron County, WI, on 3 May 2019. Photograph © Stephen E. Anich.

Figure 2. Two Nymphalis antiopa (Mourning Cloak) pursuing an Eptesicus fuscus (Big Brown Bat) near Upson, Iron County, WI, on 3 May 2019. Photograph © Stephen E. Anich.

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taken as visual evidence of the observation, and species experts later identified the animals pictured. The relatively large size, dark coloring, and light-yellow margin of the butterfly are diagnostic for Mourning Cloak, which is among the earliest butterflies to emerge from hibernation in this region (N.M. Anich, pers. observ.; J. Watson, Wisconsin Department of Natural Resources, Madison, WI, and M. Reese, Two Rivers, WI, pers. comm.). J.P. White and H. Kaarakka (Wisconsin Department of Natural Resources, Madison, WI) identified the Big Brown Bat based on diagnostic wing shape and approximate body size. Based on the Mourning Cloak size (~8 cm), the bat appears too large to have been the other bat species known to occur in the area (Kurta 2017), such as Myotis lucifugus (Le Conte) (Little Brown Bat) or Lasionycteris noctivagans (Le Conte) (Silver-haired Bat). The Big Brown Bat is also among the earliest bats to emerge from hibernation in this region. The images reliably show 1 Mourning Cloak, and in one of the images 2 Mourning Cloaks, posteriorly positioned within 1 m of the Big Brown Bat, regardless of the bat’s angle or trajectory (Figs. 1, 2). Air temperature at the time of the observation was 14.4 °C, which was warmer than the previous 5 days (when the temperature varied from -6.1 to 10.0 °C [average = 4.1 °C]). The sky was partly cloudy with no precipitation (weather data from station KIWD, Ironwood, MI [25 km away]; Wunderground 2019). Discussion. It is adaptive for butterflies to exclude conspecifics or other butterflies from territories because the territory holder is attempting to control rendezvous sites where they are likely to encounter females (Baker 1972, Benson et al. 1989) or quality foraging sites (Rocha and Duarte 2001). However, it appears in some cases that butterflies are unable to discriminate among different types of flying objects and are therefore inclined to pursue anything that resembles their intended target. Bitzer and Shaw (1983) noted that Mourn-ing Cloaks were apparently unable to even tell the sex of conspecifics until they prodded the intruder, and if the intruder flipped its wings, the territory holder could recognize the sex. Benson et al. (1989) reported the butterflies Eueides tales (Cramer) and Heliconius sara (Fabricius) (Sara Longwing) also pursued non-butterflies, apparently triggered by the movement of falling leaves, birds, and other insects through the airspace of their territory. Heterospecific territoriality has also been observed in other orders of insects. For example, Schultz and Switzer (2001) documented territorial Perithemis tenera (Say) (Eastern Amber-wing) defending their territories against other odonates, plus a horsefly (Tabanus sp.) and a butterfly (Ancyloxypha numitor) (Fabricius) (Least Skipper). Territory size for Mourning Cloaks has been reported as averaging 308 m2 (28–43 m by 6–13 m; SD = 124.7, n = 5; Bitzer and Shaw 1983). Given the route over which the bat seemed to be flying, it likely entered 1 or 2 Mourning Cloak territories. As previously stated, causal reasons for daytime activity in bats are varied (Bartonička and Řehák 2007, Bernard and McCracken 2017, Boyles et al. 2006, Davis and Hitchcock 1965, Downs et al. 2015, Kunz 1974, Sparks et al. 2003, Speakman 1990, Speakman and Racey 1989). The observation occurred on the opening weekend of fishing season—the first weekend with much human activity around cabins that were seldom used during winter—suggesting the Big Brown Bat was active due to human disturbance of bats roosting in or near one of the cabins or outbuildings. It is also possible the bat was taking advantage of the warm weather to forage. The apparent risk of predation of the Mourning Cloak by the Big Brown Bat during this observation begs the question: Does this behavior represent an evolutionary trade-off between aggressive behavior and mortality risk? It is well-known that butterflies and moths are specially adapted to detect sounds that are generated by predators (Fournier et al. 2013), but since Mourning Cloaks are day-active, their ears are likely sensitive only to day-active

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predators which often emit lower frequency sounds (Hall 2014). Mourning Cloaks may lack the ability to effectively detect higher frequency sounds like those that are commonly emit-ted by Big Brown Bats, leaving the Mourning Cloaks potentially vulnerable to this predator. Even if Mourning Cloaks could detect sounds from bats, they may not register in a situa-tion where the Mourning Cloak is posterior to the bat. Furthermore, the Mourning Cloak may not even recognize bat vocalizations as a threat, given limited contact with nocturnal species. Several studies across the range of the Big Brown Bat have listed Lepidopterans among the major prey types, indicating Mourning Cloaks are certainly a possible prey item (Agosta 2002, Clare et al. 2014, Hamilton and Barclay 1998), although analysis of guano from Big Brown Bats at 10 sites in Wisconsin from 2014–2015 did not reveal the presence of Mourning Cloaks nor any representative from the family Nymphalidae (A. Wray, Univer-sity of Wisconsin, Madison, WI, unpubl. data). Furthermore, the differing periods of normal activity between bats and Mourning Cloaks reduces the possibility of regular interactions and makes it unlikely that butterflies end up pursuing bats often. Indeed, we were unable to find another report in the literature of a butterfly pursuing a bat. An alternate explanation is that the position of the butterfly behind the bat serves to pro-tect it from possible predation, and potentially alert other species to the presence of the bat. In other taxa such as birds, mobbing can serve as an anti-predator strategy (Pettifor 1990). However, these types of social defense strategies are not known in butterflies. The fact that butterflies will even follow falling leaves seems to indicate their predisposition to simply pursue any moving object in their territory is the most likely explanation for this event. Acknowledgments. We would like to thank Harold Greeney for providing important life history information. Heather Kaarakka, Jay Watson, John Rawlins, and 2 anonymous reviewers provided comments that improved this manuscript.

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