trophic ecology of two raptors, barn owl (tyto alba) and ...

The Wilson Journal of Ornithology 128(2):385–397, 2016

TROPHIC ECOLOGY OF TWO RAPTORS, BARN OWL (TYTO ALBA) AND WHITE-TAILED KITE (ELANUS LEUCURUS), AND POSSIBLE IMPLICATIONS FOR BIOLOGICAL CONTROL OF HANTAVIRUS RESERVOIR IN CHILE ˜ OZ-PEDREROS,1,5 CLAUDIA GIL,2 JOSE´ YA Ń ˜ EZ,2,3 ANDRE´S MUN 2,4 2 ¨ LLER JAIME R. RAU, AND PATRICIA MO ABSTRACT.—Raptors are important predators of various species of small mammals, which renders them of economic importance since their prey may be either disease vectors or reservoirs which represent health problems, or economically important through the damage they cause to crops and stocks. The long-tailed rice rat Oligoryzomys longicaudatus is a reservoir and vector of Hantavirus, a disease of increasing importance in various Latin American countries. The nocturnal Barn Owl (Tyto alba) and the diurnal White-tailed Kite (Elanus leucurus) appear to be the most significant predators of this species. Here, we characterize the diet of these two raptors and analyze their trophic specialization and dietary selectivity using published information, pellet analysis, and field abundances of small mammals. Both raptor species positively selected O. longicaudatus in their diets to suggest that they could be potential controllers of the Hantavirus reservoir in Chile, both in natural and agricultural ecosystems. Predation on O. longicaudatus by these two raptors is interesting because they have complementary activity periods, a condition which enables them to share the same prey without having strong interference. Received 6 April 2015. Accepted 17 September 2015. Key words: birds of prey, diurnal and nocturnal raptors, Elanus leucurus, Oligoryzomys longicaudatus, Tyto alba.

INTRODUCTION In general, nocturnal birds of prey can be effective predators of some species of the order Rodentia and other small mammals, which make them anthropogenically important, as many of these rodents may be harmful to forestry or agricultural activity (see Rodrı´guez 1987, MunõzPedreros and Muruá 1990). At the same time, some rodents play an important role in the epidemiology of various diseases affecting domestic animals, wildlife, and humans (MunõzPedreros and Gil 2009). Such a role has been described for the Long-tailed rice rat (Oligoryzomys longicaudatus) a reservoir and vector of Hantavirus (Pavletic 2000, Castillo and Ossa 2002, Torres-Pe´rez et al. 2004). Although this species is the only one documented as a Hantavirus reservoir in Chile to date, seropositivity of 1 Nućleo de Investigacioń en Estudios Ambientales NEA, Laboratorio de Ecologıá Aplicada y Biodiversidad, Escuela de Ciencias Ambientales, Facultad de Recursos Naturales, Universidad Cato´lica de Temuco. Casilla 15-D, Temuco, Chile. 2 Programa de Conservacioń de Aves Rapaces y Control Biolo´gico, Centro de Estudios Agrarios y Ambientales, Casilla 164, Valdivia, Chile. 3 Museo Nacional de Historia Natural. Santiago, Chile. 4 Laboratorio de Ecologıá, Departamento de Ciencias Ba´sicas and Programa IBAM, Universidad de Los Lagos, Casilla 933, Osorno, Chile. 5 Corresponding author; e-mail: [email protected]

Hantavirus has been found in other rodents such as Abrothrix olivaceus, Abrothrix longipilis, Phyllotis darwini, Loxodontomys micropus, Rattus rattus, and Rattus norvegicus (see Pavletic 2000, Ortiz et al. 2004, Lobos et al. 2005, Fernańdez et al. 2008). Oligoryzomys longicaudatus has a wide distribution in Chile extending from the Copiapo´ valley (27u S), to the Magallanes Regioń (55u S; Gallardo and Palma 1990, Belmar-Lucero et al. 2009). The transmission of the virus is an environmental and epidemiological risk to humans who come into contact with seropositive rodents. This exposure to risk is particularly relevant in rural areas where people living and visiting may be more likely to come into contact with rodent disease (Navarrete et al. 2000, Sotomayor and Aguilera 2000). The management and control of this risk can involve the predators of the reservoir of the disease (Munõz-Pedreros et al. 2010b). Some raptor species can perform an ecological role in the regulation of rodent numbers. Although it has been difficult to demonstrate this top-down control empirically (see Ostfeld and Holt 2004, Salo et al. 2010), several authors (see Norrdahl and Korpima¨ki 1996, Korpima¨ki and Norrdahl 1998, Korpima¨ki et al. 2002, Hanski et al. 2001, Gilg et al. 2003) document the impact of specialist predators, especially raptors (e.g., Falco tinnunculus, Aegolius funereus, Asio otus, and

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A. flammeus) on rodent populations (e.g., Microtus agrestis, Microtus rossiaemeridionalis and Clethrionomys glareolus), for Finland and Greenland. These species can perform an ecological role in the regulation of rodent numbers. Packer et al. (2003), Ostfeld and Holt (2004), and Hall et al. (2005) used simple models to suggest that reduction in predator numbers can increase disease incidence, and that a potentially harmful consequence of predator removal could be enhanced “spillover” infection to novel host species, including humans (Roy and Holt 2008). In addition to the specialist predators, the generalists also appear to have a role in protecting human health through the chronic suppression of populations of rodents, helping to keep their densities low (Ostfeld and Holt 2004). Birds of prey that can potentially be agents harvesting the Hantavirus reservoir should, if possible, meet the following requirements (Munõz-Pedreros et al. 2010b): (a) intake of a high number of individuals of the target species; (b) selective consumption of this species; (c) activity periods that overlap with that of the target species; and probably be : (d) relatively abundant in the focal area; and (e) relatively large, since body size and energy requirements are positively correlated, in absolute terms (see Bozinovic and Medel 1988). Some, or all of these criteria, must have a negative impact on the population growth of the target species, although this effect would not necessarily be caused by one or two raptors species but by different species in different locations in distributional range of the reservoir. The replacement of native vegetation and the traditional management by intensive agriculture are happening very quickly in Chile (Echeverrıá et al. 2006, Carmona et al. 2010) and may have a negative effect on birds. Habitat heterogeneity is a key process to maintain diversity in agricultural landscapes (Gavier-Pizarro et al. 2012), although raptors are affected differently depending on their physical and temporal (nocturnal or diurnal) use of habitat, the availability of shelter, nesting sites, and food (Butet et al. 2010, Goulart et al. 2013). According to the above criteria (in MunõzPedreros et al. 2010b), two raptor species in Chile that potentially could harvest the Hantavirus reservoir, meet most requirements described: the Barn Owl (Tyto alba), with nocturnal activity, weight of 390–450 g, and size of 36–38 cm, and the White-tailed Kite (Elanus leucurus), with diurnal-crepuscular activity, weight of 250–300 g,

and size of 40–44 cm (Pavez 2004). Both species occupy agroecosystems. The diets of nocturnal raptors (Order Strigiformes) are relatively welldocumented in Chile (see Jaksic 1997). However, attention has not been focused on the selective consumption of prey which are also human disease reservoirs, except for Munõz-Pedreros (2004) who suggests the potential regulating effect of the Barn Owl on populations of O. longicaudatus. The objectives of this study are: (a) to characterize the diet of these two raptors in a latitudinal transect, with special focus on dietary selectivity on O. longicaudatus, and, (b) to consider their possible role as biological controllers of this rodent. METHODS Study Areas.—We analyzed the available information on diets for both species of raptors, from 24 localities in Chile from 30u 389 S to 51u 039 S, (Fig. 1). Availability of prey was evaluated only for the (RN) Lago Pen˜uelas. These localities have been located and analyzed as ecoregions. The biogeographic classification most used in Latin America and the Caribbean is that of Dinerstein et al. (1995) and Olson et al. (2001), which recognizes twelve ecoregions in Chile. The study localities fall into three ecoregions: (a) the Chilean Matorral represented by 13 locations between 30u 389 S and 36u 349 S (Parque Nacional Fray Jorge to Chillań); (b) the Valdivian temperate forest, represented by four locations between 38u 369 S y 40u 349 S (Carriel Sur to Osorno) and (c) the Subpolar Nothofagus forest with only one location 51u 039 S (National Park Torres del Paine). The information on the diet of T. alba where it exceeds the northern geographical range of O. longicaudatus (27u S) (e.g., Jaksic et al. 1999 at 22u 189 S, Carmona and Rivadeneira 2006 at 20u 519 S), was not included. In two of the 24 localities, pellets were collected to complement dietary studies, and in one location information was obtained on the abundance of small mammals in the field. The areas where pellets were collected were: (a) the National Reserve (RN) Lago Pen˜uelas (33u 079 S and 71u 249 W) in central Chile, with three communities of natural vegetation: an Acacia caven (Molina) Molina and Maytenus boaria Molina savannah; a sclerophyllous forest of Peumus boldus Molina, Quillaja saponaria Molina and Cryptocarya alba (Molina) Looser, and a mixed shrub of A. caven and

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FIG. 1. Study area. Dots indicate sampling localities.15 Puchuncavı´, 25 Los Maitenes, 35 PN La Campana, 45 RN Lago Pen˜uelas, 55 Polpaico, 65 El Pangue, 75 Las Vizcachas, 85 La Dehesa, 95 Los Domıńicos, 105 Pudahuel.

Baccharis linearis (Ruiz et Pav.) Pers; exotic vegetation pine stands of Pinus radiata (D Don) and eucalyptus Eucalyptus globulus Labill. are present in the area (see details in Hauenstein et al. 2009); and (b) a 280 ha private property in Las Vegas de Cholchol (38u 369 S; 42u 249 W) southern Chile, containing 192 ha of E. globulus plantations, 18 ha of native forest of C. alba and P. boldus, and the remaining area tilled soil. Methods.—We calculated trophic statistics with data when analyzed publications were not provided in these studies. The pellets analyzed were collected from September 2001 (late winter) to March 2004 (late autumn) in the stated areas. The methodology to process the owl pellets followed Munõz-Pedreros and Rau (2004), procedures for

identifying the material followed Reise (1973), the taxonomy of birds and mammal prey followed Torres-Mura (2004), and Yań˜ez and MunõzPedreros (2009). Statistical Analyses.—To characterize the diet, we used the following trophic statistics: (a) Geometric mean of the average weight of prey consumed, which was obtained by adding the products of the numbers of individual prey times of its mean weight (log 10), divided by the total number of prey items used in the calculation. The average weights of prey items were obtained from field data taken at the same time as pellet collections and from bibliographic information for other locations; (b) Simpson’s reciprocal measure (Simpson 1949) or Levins’ index:


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B 5 1= Sni~1 p2i where p1 is the relative occurrence of prey taxon i in the diet of a given species. For this, we used highest resolution of taxonomic categories of vertebrate prey to species level; invertebrate preys were excluded. The values for the trophic niche breadth range from 1 (when only one category of prey was consumed) to n (when all categories of prey are equally consumed); (c) standardized Levins’ index according to Colwell and Futuyma (1971) which was used to compare different locations in which prey supply may be different. Bsta fluctuates between 0–1. Bsta 5 (Bobs 2 Bmin)/(Bmax 2 Bmin), where, Bobs is the observed trophic niche breadth (Levins’ index), Bmin is the minimum possible trophic niche (5 1), Bmax is the maximum possible trophic niche (5 n, is the number of prey taxa actually consumed by a particular species of raptor). A value of 0 indicates a diet specialist and a value of 1 maximum diet generalist; (d) Diet selectivity, calculated according to the formula for more than two kinds of prey in the diet of raptors, for those areas where prey abundance was obtained by trapping: X 25g(fo2fe)2/fe where fo 5 observed frequency of prey item found in the pellets, fe 5 expected frequency of prey items obtained by trapping (Jaksic 1979). To estimate prey abundance in RN Lago Pen˜uelas, seasonal small mammal trapping was conducted using 144 Sherman collapsible traps, baited with crushed oats (see Munõz -Pedreros et al. 2010a). This study was conducted on the same month and year that the pellets were analyzed. RESULTS AND DISCUSSION Diet of Tyto alba.—Table 1 presents the results of the content analysis of 4,182 pellets in the latitudinal transect covering from 30u 389 S to 51u 039 S. In RN Lago Pen˜uelas (this study), the most frequently consumed rodent was A. olivaceus, followed by A. longipilis, Abrocoma bennetti Waterhouse, 1837 and O. longicaudatus. This differs from what Maldonado (1986) documented in the same area, in which the most consumed prey was O. longicaudatus followed by A. olivaceus and A. longipilis. The variation of O. longicaudatus is explained since their populations have biannual abundances and are susceptible to climatic variations (Muruá et al. 1986, Muruá. et al. 2003, Gonza´lez et al. 1989, Muruá and Briones 2005). With respect to the trophic niche breadth, maximum values were obtained in four location of central Chile 32u 579 S to 36u 349 S (Cholchol,

PN La Campana, El Pangue and Chillań), and the lowest values were for southern Chile at 39u to 40u S. In the ecoregion of the Chilean Matorral, T. alba shows a major consumption of O. longicaudatus in six localities 32u 459 S to 34u 369 S), where this species of rodent is the most important prey, followed by Phyllotis darwini (Jaksic and Yań˜ez 1979). For National Park (PN), La Campana, Zunino and Arcos (1989) postulate alternative explanations noting that the dietary selectivity in T. alba for A. bennetti and Octodon lunatus appears to be related to the size of rodent prey, while the high proportion of O. longicaudatus in the diet could be explained by its abundance and ease of capture because of the displacement by jumps of this rodent (Va´squez 1994). Near Chillań, Gonza´lez Acunã et al. (2004) document that O. longicaudatus was the most consumed prey followed by A. olivaceus. In other sites of the Chilean Matorral ecorregion (e.g., Fray Jorge, Termas del Flaco, RN Queules, and Burca), O. longicaudatus is not among the two most consumed prey, and it will be interesting to establish if the pattern of abundance of this species shows latitudinal variations in Chile. Farther south in the Valdivian temperate forest ecoregion in the Cholchol locatily, O. longicaudatus was the most consumed prey followed by A. olivaceus similar to the findings for Lastarria by Rau et al. (1985). For Valdivia, Simeone (1995) documented that O. longicaudatus was the most consumed prey, both in samples from 1974–1979 and from 1990–1992, followed by A. olivaceus for both periods. In Osorno, Figueroa et al. (2009) showed that the most consumed preys in winter were A. olivaceus and O. longicaudatus. In the locality of the Subpolar Nothofagus forest ecoregion (National Park Torres del Paine) the most consumed prey is A. olivaceus followed by Reithrodon physodes (Olfers, 1818) and then by O. longicaudatus (Iriarte et al. 1990). Although Iriarte et al. (1990) identified the species recorded in the pellets of T. alba as O. magellanicus, we presume they correspond to O. longicaudatus. Belmar-Lucero et al. (2009) extend the distributional range of the latter species to at least 55u S, suggesting that the southern population corresponds to O. longicaudatus and that O.magellanicus probably is restricted to the type locality. Dietary Selectivity of T. alba.—The X2 test for theRN Lago Pen˜uelas indicated that T. alba did


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not consume all vertebrate prey in the same proportion in which they were present in the area (X2 5 3.841 P 5 0.05; Table 2). Significant differences were detected for A. olivaceus, Octodon degus (Molina, 1782), and R. norvegicus, which were negatively selected or rejected, and O. longicaudatus, A. bennetti and A. longipilis, which were positively selected or preferred. We detected no statistically significant differences for the consumption of R. rattus or for the cluster of species formed by O. lunatus, P. darwini and Spalacopus cyanus. The latter prey was consumed randomly or proportionally to availability. Cerpa and Yań˜ez (1981) suggest that T. alba in central Chile (32u 449 S Puchuncavı´) exhibits dietary selectivity, since it consumes only some of the prey species that inhabit the area, presenting an annual consumption of 78.2 % of rodents, mainly O. longicaudatus (35.2 % of all rodents). The results obtained by these authors suggest an optimal size of prey consumed, indicating that selection is by prey size, as the most consumed prey approaches the average size of the predominant rodent prey in the diet. Accordingly, in central-south Chile (Burca, Concepcioń 36u 329 S), in P. radiata plantations with dense brush, Munõz-Pedreros and Muruá (1990) concluded that T. alba was a selective predator of Octodon bridgesi and P. darwini, although the former is larger than the optimum size determined for this owl. These results are consistent with information provided by Fulk (1976), who noted that T. alba consumed P. darwini disproportionally to abundance in the environment (Fray Jorge 30u 389 S). In contrast, Ebensperger et al. (1991) in El Pangue (33u 179 S) indicate that T. alba preys on small mammals, behaving as an opportunistic predator which captures its prey depending on environmental supply. Sympatric studies have determined that the average size of rodent prey increases with the size of the raptor, thus T. alba captures smaller prey than Bubo magellanicus. These differences, however, are not always statistically significant (Jaksic and Yań˜ez 1980, Iriarte et al. 1990). In Torres del Paine, 99.8% of the diet of T. alba were rodents (Iriarte et al. 1990). This apparent selectivity may be a result of behavioral aspects of both prey and of this strictly nocturnal predator. Iriarte et al. (1990) conclude, like Jaksic and Yań˜ez (1980) and Simonetti Z. and Walkowiak B. (1979), that T. alba is a rodent specialist predator that preys more heavily on nocturnal small mammals than on diurnal or crepuscular rodents. However, at RN

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Lago Pen˜uelas, Maldonado (1986) proposed that T. alba is not only a specialist predator of nocturnal rodents but also of crepuscular ones. Diet of Elanus leucurus.—Considering all available information, at five locations (n 5 1,911 pellets), this raptor has a very high consumption of rodents, being the most consumed prey A. olivaceus and O. longicaudatus (Table 3). In the Chilean Matorral ecoregion, the maximum values of trophic niche breadth were obtained for Pudahuel and La Dehesa, and the lowest were at Polpaico where Meserve (1977) documented that A. olivaceus constituted more than 75% of White-tailed Kites’ diet. Schlatter et al. (1980) documented the diet of E. leucurus in Pudahuel in an area with high levels of human disturbance and in La Dehesa with low disturbance. The authors explain the high proportion of O. longicaudatus in the diet by the occurrence of a mouse outbreak (see Jaksic and Lima 2003) during the study period and by the high vulnerability and abundance of this rodent in areas of high human disturbance. In the Valdivian temperate forest ecoregion Carriel Sur, a suburban area dominated by wet meadows, Gonza´lez-Acunã et al. (2009), found that the most consumed preys were A. olivaceus and A. longipilis. The frequency of species of rodent prey in the pellets were associated positively with their abundances in the field (rs 5 0.83, P , 0.05); therefore, the authors concluded that E. leucurus is a specialist on rodents and an opportunistic predator. Farther south, but in the same ecoregion in agricultural ecosystems within the urban area of Valdivia, Simeone (1995) found that the most important prey was O. longicaudatus followed by A. olivaceus (Table 3). Thirty years later, from 1990–1992, the proportion for O. longicaudatus increased, reaching .45%, at the same site, which showed a marked increase in human disturbance. Although O. longicaudatus is considered nocturnal, it is evident that it also has crepuscular activity, which enables predation by the Whitetailed Kite, a diurnal raptor with crepuscular activity (Pavez 2004). Impact on Pest Populations.—Published information documents a geographic expansion of Hantavirus pulmonary syndrome (Bellomo et al. 2009), showing that there is flow of virus throughout the distribution area of the reservoir (Padula et al. 2000, Pavletic 2000), ranging from 1–40% seroprevalence for Latin America and


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Thylamys elegans Dromiciops gliroides Non determined Chiroptera Tadarida brasiliensis Oligoryzomys longicaudatus Abrothrix sp. Abrothrix longipilis Abrothrix olivaceus Geoxus valdivianus Chelemys macronyx Chelemys megalonyx Eligmodontia typus Phyllotis darwini Phyllotis xanthopygus Phyllotis vaccarum Phyllotis sp. Loxodontomys micropus Reithrodon physodes Euneomys chinchilloides Octodon bridgesi Octodon degus Octodon lunatus Spalacopus cyanus Aconaemys fuscus Abrocoma bennetti Rattus rattus Rattus norvegicus Rattus sp. Mus musculus Non determined cricetids Non determined rodents Oryctolagus cuniculus Total Mammals Non determined Passeriformes Anseriformes Non determined birds Total Birds Non determined reptiles Total Reptiles TOTAL VERTEBRATE PREY TOTAL PELLETS Bobs Bst

Locations: Latitude: Longitude: Source: ITEM:


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10

37 300 40

31,2 40 12 12 30,3 30 52,5 29,9 50 55,4 55,5 17 57,3 63 65 57 64,8 76,3 55,5 170,6 160,6 142,1 84 155 233,5 158 93,3 120 15,9 48,5 84,2 180

Mass (g)

292 195 2,77 0,22

100,0

4,5 0,3 0,3

1,0

5,8 5,8 0,6 0,6 310 95 4,76 0,34

93,5

2,6

1,9 16,5

0,3 0,6 2,3

13,2

0,3 22,9

49,0

32,9

6,8

Puchuncavı´ 32u 449 S 71u 249 W 2 F%

0,3 33,6

4,1

PN Fray Jorge 30u 389 S 71u 409 W 1 F%

332 239 3,80 0,23

1,2 1,2

0,9 0,3 98,8

4,8

0,9

0,6 7,8

5,4

34,0

0,6 6,9

36,1

0,3

Los Maitenes 32u 469 S 71u 279 W 3 F%

129 101 6,71 0,63

1,6 1,6

98,4

18,6

24,0

5,4 14,0

8,5

0,8 5,4

11,6

10,1

32u 579 S 71u 089 W 4 F%

PN La Campana

1,348 1,035 6,32 0,48

4,2 4,2

95,8

9,3

3,7 8,0

0,6

5,4

16,7

12,0 5,6

30,0

1,0

3,4

Central Chile a 32u 459–34u 369 S 70u 319–71u 34O 5 F%

12,1 12,1 0,2 0,2 447 228 7,00 0,40

6,5 2,0 87,7

0,2

10,1 2,5

0,2 2,2 2,2

2,0

0,2

13,2 17,9

24,6

3,8

RN Pen˜uelas 33u 079 S 71u 249 O 6 F%

134 43 6,80 0,58

0,7 0,7

20,9 6,7 3,0 99,3

6,0

0,7

1,5

11,9

13,4

18,7

16,4

El Pangue 33u 179 S 71u 119 0 7 F%

565 351 4,04 0,30

107,4 5,2

10,2

12,7 1,8

1,0

2,0

40,8

9,4 1,8

17,9

9,8

La Dehesa 33u 219 S 70u 329 0 8 F%

91 76 5,91 0,41

96,7 3,3

5,5

6,6

53 39 2,18 0,29

100,0

17,0

352 318 6,47 0,46

1,1 1,1

0,6 0,9 98,9

1,7

9,7

2,0

17,0

1,1 5,5

0,6

20,5

11,1 10,8

22,2

2,0

El Alamo 36u 119 S 72u 249 O 11 F%

3,3 3,3

13,2

64,2

1,9

3,8

RN Los Queules 35u 599 S 72u 419 O 10 F%

11,0

35,2

3,3

3,3 9,9

8,8

Banõs del Flaco 34u 359 S 71u 009 O 9 F%

TABLE 1. Diet composition of T. alba in 18 localities in Chile. F% 5 Frequency of prey, B% 5 Frequency of biomass.

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109 103 3,29 0,46

100,0

1,4

12,9

84 47 6,17 0,74

4,8

12,8

609 259 4,04 0,51

95,2 4,8

9,5 13,1

14,3

3,6

10,7 17,9

26,2

Chol Chol 38u 369 S 72u 429 O 14 F%

87,2 12,8

7,6

8,2

8,4

7,2 12,0

5,8 31,7

42,4

43,8

Chillań 36u 349 S 72a06O 13 F%

5,8

Burca 36u 329 S 79u 559 O 12 F%

131 56 3,52 0,31

100,0

3,1

5,3

0,8

2,3

6,9 9,2

2,3 25,2

45,0

Lastarria 39u 139 S 70u 309 O 15 F%

TABLE 1. Extended.

980 467 2,85 0,12

5,0

95,0 4,9 0,1

1,5 5,1 4,1 0,5

3,3

0,1 55,4 1,6 4,9 18,4

0,1

Valdivia 39u 489 S, 73u 109 O 16 F%

303 228 2,76 0,20

100,0

14,8

3,4 0,4

1,5

0,2 9,2

1,3 56,0 0,4

12,7

Osorno 40u 349 S 73u059 O 17 F%

531 302 5,45 0,49

2,5

99,8 2,5

8,7

13,7 19,6 1,7

3,2

5,1

2,4

15,3 30,1

PN Torres del Paine 51u 039 S 72u559 O 18 F%

2,42 0,01 0,20 0,01 28,77 2,52 6,45 14,56 0,03 0,23 0,01 0,39 12,73 0,24 0,46 0,73 2,72 1,49 0,21 1,26 1,39 0,46 0,92 0,01 3,09 3,60 0,76 1,10 3,90 0,40 4,36 0,24 95,7 2,29 0,01 1,99 4,29 0,04 0,04 6,800 4,182

Total F%

1,33 0,01 0,04 0,00 15,36 1,33 5,97 7,67 0,03 0,22 0,01 0,12 12,85 0,27 0,52 0,73 3,10 2,00 0,21 3,78 3,93 1,15 1,35 0,04 12,71 10,03 1,25 2,33 1,09 0,34 6,47 0,77 97,0 1,49 0,08 1,40 2,97 0,01 0,01

B%

Includes six locations. Source: 15 Fulk 1976; 25 Cerpa and Yań˜ez 1981; 35 Begall 2005; 45 Simonetti and Walkoviak 1979; Zunino and Arcos 1989; 55 Jaksic and Yań˜ez 1979; 65 Jaksic and Yań˜ez 1979; Maldonado 1986; this study; 75 Ebensperger et al. 1991; 85 Reise 1970; Jaksic and Yań˜ez 1980; 95 Torres-Mura and Contreras 1989; 105 Correa and Roa 2005; 115 Begall 2005; 125 Munõz and Muruá 1990; 135 Gonza´lez Acunã et al. 2004; 145 this study; 155 Rau et al. 1985; 165 Simeone 1995; 175 Figueroa et al. 2009; 185 Iriarte et al. 1990.

a

Thylamys elegans Dromiciops gliroides Non determined Chiroptera Tadarida brasiliensis Oligoryzomys longicaudatus Abrothrix sp. Abrothrix longipilis Abrothrix olivaceus Geoxus valdivianus Chelemys macronyx Chelemys megalonyx Eligmodontia typus Phyllotis darwini Phyllotis xanthopygus Phyllotis vaccarum Phyllotis sp. Loxodontomys micropus Reithrodon physodes Euneomys chinchilloides Octodon bridgesi Octodon degus Octodon lunatus Spalacopus cyanus Aconaemys fuscus Abrocoma bennetti Rattus rattus Rattus norvegicus Rattus sp. Mus musculus Non determined cricetids Non determined rodents Oryctolagus cuniculus Total Mammals Non determined Passeriformes Anseriformes Non determined birds Total Birds Non determined reptiles Total Reptiles TOTAL VERTEBRATE PREY TOTAL PELLETS Bobs Bst

Locations: Latitude: Longitude: Source: ITEM:


391

392


TABLE 2. Relative abundance of micro mammals in the RN Lago Pen˜uelas and values of X2 for the vertebrate prey consumed by T. alba. (X2 5 3.841 P 5 0.05).* 5 significant differences. Species

Abrothrix olivaceus Octodon degus Oligoryzomys longicaudatus Rattus norvergicus Abrothrix longipilis Abrocoma bennetti Rattus rattus Thylamys elegans Octodon lunatus Phyllotis darwini Spalacopus cyanus Mus musculus Total

Frequency

Relative abundance

X2

88 29

40.37 12.84

11.159* 26.155*

22 20 16 14 14 11 4 3 0 0 221

10.09 8.26 7.34 6.42 6.42 5.05 1.83 1.38 0 0 100

16.170* 18.089* 59.496* 63.757* 1.821

23.930

from 1.7% to 13% in Chile (Puerta et al. 2006). In Argentina, 8% prevalence is documented (Calderoń et al. 1999, Cantoni et al. 2001) and 4% in Paraguay (Yahnke et al. 2001). Regarding the population fluctuations of the reservoirs, Muruá et al. (2003) found no significant correlation between annual seroprevalence in O. longicaudatus with total abundance indices for each year for the species (Pearson correlation coefficient 5 0.82 and 0.88, P 5 0.179 and P 5 0.118 respectively). However, by relating the index of abundance of O. longicaudatus with the number of seropositive individuals for Hantavirus, they found a significant correlation (Pearson correlation coefficient 5 0.95, P 5 0.045). Thus, the intake of the Hantavirus reservoir by raptors has an impact on seropositive individuals. T. alba ingests from 50–150 g of food daily, equivalent to the consumption of 1–3 mice during this period of time. If we consider a family of two adults and four nestlings, they will consume 16–18 mice per day, totaling around 1,000 individuals during the 10-week period of nesting (see Marti 1973, 1992; Colvin 1985). In RN Lago Pen˜uelas, gross density of T. alba was 2.13 individuals/km2, after 2 years of habitat improvement for this species (Munõz-Pedreros et al. 2010b). So, considering an intake of three mice per day per owl, we estimated an annual rodent consumption of 2,332 individuals/km2 in the year 2003. We have no information on rodent density for this area, but in a similar ecosystem in San Carlos de Apoquindo

(33u 239 S, 70u 319 W), Iriarte et al. (1989) estimated a small mammal density of 5,790 individuals/km2. Thus, the impact that Barn Owls can have on rodent populations is significant. In conclusion, Barn Owls can be characterized at a gross level as rodent specialists that can, however, respond opportunistically at a fine level, to the availability of such prey (cf, Begall 2005). Taking in account all available information on the diet of T. alba (4,182 pellets excluding the invertebrate prey) in the distribution range of the rodent reservoir for Hantavirus, the most consumed prey is O. longicaudatus (28.77%), followed by A. olivaceus (14.56%) and P. darwini (12.73%) (Table 1). This, coupled with the selectivity studies conducted, suggests that T. alba is a potentially good biological control agent for O. longicaudatus, since it meets several of the requirements: it is a specialist predator on rodents (.90 % of their diet), with selective intake of the target species (.28 % of their diet); overlapping nocturnal period of activity; and has relatively large body size. On the other hand, E. leucurus is a specialist predator on rodents (.97%) with a generalist strategy (see Scheibler 2004), which has potential as a biological control agent of O. longicaudatus when it is abundant in the environment.Further, it is diurnal with crepuscular activity, so in those areas where it coexists sympatrically with T. alba, the two species could share the same resource (target species), without experiencing interference competition (see Greene and Jaksic 1983). Regarding other nocturnal birds of prey, most authors suggest that Bubo magellanicus is a specialist predator on rodents (61.71% with O. longicaudatus, 12.4% being the most consumed prey), which shifts to a generalistic strategy on other prey in periods of population decrease of rodents (spring-summer), thus enabling the inclusion of insects and lagomorphs in its diet (Yań˜ez and Jaksic 1977; Jaksic et al. 1978, 1986; Yań˜ez et al. 1978; Jaksic and Yań˜ez 1980; Rau and Yań˜ez 1981; Iriarte et al. 1990; Tala et al. 1995; AM-P, unpubl. data). Strix rufipes deserves special attention as its consumption of O. longicaudatus varies from Central Chile (33u 469 S) to South Chile (40u 409 S) from 3.9–60.3% (Martıńez 1993; Martıńez and Jaksic 1996, 1997; Dıáz 1999). So the above mentioned raptor species can form functional guilds and coexist in sympatry with other raptors.


392

ITEM:

Oligoryzomys longicaudatus Abrothrix longipilis Abrothrix olivaceus Abrothrix sp. Phyllotis darwini Loxodontomys micropus Octodon degus Rattus norvegicus Rattus rattus Rattus sp. Mus musculus Non determined rodents Total Mammals Tirannidae Non determined Passeriformes Troglodytidae Non determined birds Total Birds Liolaemus sp. Total Reptiles TOTAL VERTEBRATES Carabidae Curculionidae Scarabaeidae Tenebrionidae Bostrichidae Blattidae Non determined Coleoptera Non determined Orthoptera TOTAL INVERTEBRATES TOTAL PREY TOTAL PELLETS Bobs Bst 1 1 1 1 1 1 1 1

10

40 40 40

30.3 52.5 29.9 30 57.3 64.8 160.6 93.3 158 120 15.9 0.7

Polpaico 33u 09 S, 70u 479 O Meserve, 1977 Mass (g)

766 474 1,6 0,12

151 136 3,59 0,43

100.0

2.0 2.0

718 551 3,77 0,55

100.0

2.8 2.8

24.1 0.3 97.2

5.0 98.0

20.2 6.6 100.0

35.2

27.7

Carriel Sur 36u 469 S, 73u 039 O Gonza´lez-Acunã et al., 2009 F%

5.2

8.6

1.3

37.1 9.9 34.4

Pudahuel 33u 269 S, 70u 479 O Schlatter et al., 1980 F%

1.2

0.8 0.7 76.5

La Dehesa 33u 219 S, 70u 329 O Schlatter et al., 1980 F%


393

3.9 343 209 2,68 0,24

96.1 0.9 0.6 0.9 0.9 0.3 0.3

0.6

0.6

0.3 0.0 95.5

0.9

2.6 32.3 47.5 11.6

Valdivia 40u 359 S, 73u 109 O Simeone, 1995 F%

0.7 0.6 1.3 704 541 3,52 0,21

42.8 6.7 26.8 5.1 0.0 12.1 0.0 0.3 0.6 1.3 0.1 1.94 95.7 1.3 0.9 0.6 0.0 2.7 0.3 0.3 98.7

F%

TABLE 3. Diet composition of E. leucurus in five localities of Chile. F% 5 Frequency of prey, B% 5 Frequency of biomass.

F%

97.46 0.34 0.30 0.15 0.86 1.64 0.07 0.07 99.18 0.11 0.07 0.11 0.11 0.04 0.04 0.19 0.15 0.82 2,282 1,911

21.29 6.64 46.35 2.83 0.07 3.17 0.48 1.79 0.26 0.34 12.30

B%

0.97 0.02 0.02 99.97 0.00 0.00 0.00 0.00 0.00 0.00 0.01 0.00 0.03

98.98 0.42 0.37 0.18

19.98 10.79 42.92 2.63 0.13 6.36 2.41 5.17 1.28 1.25 6.06


393

394


Final Considerations.—In the agricultural environment prevailing in central and southern Chile, the role as biological control agents of T. alba and E. leucurus, is potentially significant in environments with abundance of Hantavirus reservoirs (Munõz-Pedreros et al. 2010b). Even though it is clear that these two species have a considerable intake of O. longicaudatus throughout Chile, this does not necessarily mean that they are the controllers of the rodent populations, although they can certainly contribute to reduced risk of human exposure to the disease reservoir. In open fields, B. magellanicus, in nearby wetlands A. flammeus, and in native forests and fragments of secondary growth forest S. rufipes, are potentially important. Finally, the records of seropositive individuals for Hantavirus of exotic murine rodents (M. musculus, R. norvegicus, and R. rattus) suggest that these constitute an environmental hazard, and more epidemiological research is needed. In this sense, raptors also contribute to the mitigation of this risk since the genus Rattus and Mus constitute 9.36% of the documented diet of T. alba (15.7% as biomass), 14.69% of the diet of E. leucurus (13.76% as biomass) (AM-P, unpubl. data). ACKNOWLEDGMENTS The authors thank the Direccioń General de Investigacioń y Postgrado, Universidad Cato´lica de Temuco, Project. CD2010 DGIPUCT-01 and Project MECESUP 0804 UCT; the Centro de Estudios Agrarios y Ambientales CEA project CHI/01/G09 Project GEF / PPS / United Nations Development Programme and the National Forestry Corporation (CONAF) Valparaı´so Region for logistical support and collaboration in the follow up of the study. They also thank S. Fletcher, J. Meza, A. Fontaine, S. Huaiquinao, R. Sanhueza, V. Riquelme, J. Rivera, and L. Corte´s for their contributions at various stages of field and laboratory work.

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