BlOTROPlCA 29(4): 522-525 1997

Weevil Larvae Dispersal by Guans in Southeastern Brazil'

Key words: Revena; seed dispersal; Syagrus; weevil.

bird-insect interactions; Brazil; Coleoptera; figivory; insect seed predation; palm; Penelope;

THE possibility that seed-predatory insect larvae could survive after passage through the guts of frugivorous birds was first suggested many years ago (Chung & Waller 1986). Increasing evidence in favor of this phenomenon has since been reported (Jordan0 1989, Traveset 1993, and references therein), and its potential relevance to insect life-history strategies has been examined (Sallabanks & Courtney 1992). Only recently, however, have quantitative studies been undertaken. Nalepa and Piper (1 994) described the survival of the larvae of a wasp (Megastipus acukatus nigrofivus) after the passage of parasitized seeds of Rosa multiji'ora through the digestive tract of caged mockingbirds (Mimwpoliglottos). Guix and Ruiz (1995) reported the survival of larvae of Revena spp. (Coleoptera: Curculionidae, Baridinae) para- sitizing fruits of the palm S y a p s romanzofiana and of a myrtaceous tree (Eugenia sp.) to stomach passage in wild toucans (Ramphastos spp.) and thrushes (Turdus rujventris).

One of the factors Guix and Ruiz (1 995) considered relevant for the high survival rate of larvae was that, owing to their relatively large size, fruits of S. romanzofiana and Eugenia sp. did not pass through the entire digestive system of the birds and, thus, their time of exposure (2-30 min) to mechanical and chemical digestive agents was considerably shortened. However, in the study by Nalepa and Piper (1994), the seed parasites survived the entire passage through the guts of frugivores.

We have observed two species of guans, Penelope obscura and I? superciliaris (Aves: Cracidae), feeding on S. romanzofiana fruits and defecating entire seeds, indicating that guans may be appropriate for testing the effects of prolonged exposure to digestive agents of a legitimate disperser on the survival of R. rubiginosa developing inside S. romanwfiana seeds. Longer retention times mean that the distances travelled by birds from the parent tree would presumably also be greater. This may enhance the dispersal efficiency of the parasite and its associated antipredatory effects (Janzen 1970), which might be a crucial factor from the parasite's point of view. We discuss our results within the conceptual framework of "evolutionary triads" involving plant-disperser-insect pest evolutionary interaction (Herrera 1984), in which each component simultaneously interacts with the other two and is able to develop adaptative or exaptative responses to such interactions.

Observations on wild guans were made at Parque Estadual da Ilha do Cardoso (25" 10' S, 48" 00' W) and at Parque Estadual Intervales (24" 20' S, 48" 15' W), both in the Atlantic rainforest of SPo Paul0 State (southeastern Brazil).

In September 1994 we performed six feeding trials to assess survival of Revena rubiginosa larvae to passage through guan guts. Each trial consisted of offering an average of 5 parasitized (scarred, see below) ripe fruits of S. romanzofiana (20-22 mm long x 15-17 mm diam.) to each of four captive Penelope obscura bronzina in the SPo Paul0 Zoological Garden. Fruits ( N = 120) containing R. rubiginosa larvae were offered in the morning (between 08:30 and 09:OO h, local time), by placing them in the aviary feeders before the birds receive their normal food. Fruits for feeding trials were selected among those that had recently fallen under S. romanwfiana palm trees at Parque Estadual das Fontes do Ipiranga (23" 36' S, 46" 38' W). To obtain parasitized fruits we inspected the fruit surface for scars indicating that a weevil larvae had entered the seed (Guix & Ruiz 1995). Fruits strongly infested with pulp feeding insects were discarded because of difficulty in recognizing R. rubiginosa scars. The fruit surface was again inspected immediately before offering the fruit to the guans to ensure that the larva had not emerged from the fruit since collection (Revena emerge from fruit as larvae and pupate in the soil; Guix & Ruiz 1995).

Guan feces were inspected every hour in search of seeds. Defecated seeds were collected and placed in glass bottles containing about 2 cm3 of soil and checked every day for larvae exiting the seeds. When larvae did not emerge after 10 days, we opened the seeds to inspect whether they actually contained larvae and whether these were alive or not.

Retention time was described using nonparametric statistics (Zar 1984). Apparent survival rates of R. rubiginosa larvae to short (regurgitated seeds) or long (defecated seeds) exposure to digestive agents

I Received 1 August 1995; revision accepted 16 May 1996.

522

Notes 523

-0 al al v) u- 0

0.7

0.6

0.5

0.3 0.41 :::I , , , , , , , \ , 0 0 1 2 3 4 5 6 7 8 9 1 0

H o u r s Elapsed

FIGURE 1. Probability of S y a p romanmfiana seeds retention in the guts of four captive Penelope obrcura as a function of the time elapsed since ingestion (N=66). An additional 12 seeds ( 1 5 % of the total) were defecated during the night more than 10 hours after they were in- gested by the guans.

were compared using contingency tables statistics (SPSS-PC) on data from trials with the toucan Ram- phastos dicolorus (Guix & Ruiz 1995) and those of the present study.

We observed groups of two or three individuals of I? obscura on seven occassions feeding naturally upon S. romanzofina fruits in Atlantic rainforest at Parque Estadual Intervales over a range of elevations from 60 to 970 m above sea level. We obtained feeding observations for I? superciliaris while monitoring a group of three individuals in lowland restinga forest at the Parque Estadual Ilha do Cardoso. We registered these animals feeding on S. romanzofiana fruits six times during 15 days. For both guan species, fruits were taken directly from clusters on trees and swallowed without mandibulation.

Of the 120 fruits offered to captive guans, 87 fruits (73%) were ingested and their seeds collected from guans excrement. Of these 87 seeds, 78 seeds (90%) had weevil larvae inside. Sixty-six (85%) of the parasitized seeds collected were excreted before sundown and 12 seeds (1 5%) were defecated during the night. For seeds excreted before sundown the median retention time was 6.24 h (Interquartile Range= 3h).

All 12 additional seeds defecated during the night had the endocarp already perforated by weevil exit holes when collected early the next morning. Hence, one or more weevils emerged and possibly survived before collecting these seeds. Of the 66 seeds maintained in glass jars, a single weevil larva emerged from 61 (92%) of them and each larva built a pupation chamber in the soil in the bottom of the bottles. The remaining five seeds (8%) were opened on day 10 and contained, in all cases, living larvae.

Since only nine (10%) scarred fruits did not contain a developed weevil larva inside, the presence of scars may be considered a reliable help to recognize S. romanmfiana fruits parasitized by R. mbiginosa.

The survival rate of 85-100% for R. mbiginosa larvae reported here demonstrate that larvae can tolerate complete passage through guan digestive tracts and that guans may be effective dispersers of this beetle. Furthermore, the hypothesis that long gut retention time may not be a critical factor to survival of this kind of seed predator is reinforced when comparing minimum survival rates of R. mbiginosa larvae to partial (regurgitated seeds) or complete (defecated seeds) passage through the guts of frugivorous birds (Table 1). The lack of significant difference (Fisher’s exact test, P = 0.73, two-tailed) probably indicates that the endocarp provides effective protection against the digestive agents of such birds.

For effective larval dispersal the frugivore must distance itself from the parent tree while retaining seeds in its gut (Guix & Ruiz 1995). The home range of Penelope superciliaris jacupemba at Ilha do Cardoso was estimated to be about 11 ha (day range between 3-7 ha; Guix & Ruiz, pers. obs.) using

524 Guix and Ruiz

TABLE 1. Minimum survival of Revena rubiginosa lar- vae parasitizing seed of Syagrus romanzoffi- ana to incomplete and complete passage through the guts of two of their legtimate dis- persers, a toucan Ramphastos dicolorus and a guan Penelope obscura. Data of survival in seed regurgitated by toucans are from Guix and Ruiz (1395). Differences not statistically signifcant (Fisher? exact test, P = 0.73, two- tailed).

Minimum survival

Yes No

Defecated seeds 66 12 78 Regurgitated seeds 22 3 25

Total 88 15 103

the minimum convex polygon method (Kenward 1987). This suggests that wild guans move far enough to disperse effectively S. romanwfiana seeds and the larvae of R. rubiginosa that the seeds may contain.

In the context of evolutionary triads (Herrera 1984), an important consideration is whether seed predators affect fruit maturation, because legitimate dispersers mainly eat mature fruits (Janzen 1977, Herrera 1982, Jordano 1989). Krischick et af. (1989) suggested that for the American holly, Zlex opaca, cecidomyid flies prevent fruit maturation and are thus not subject to mortality due to consumption by frugivorous birds. However, in other cases the interaction seems to be too weak to assume the action of natural selection, such as in the case reported by Traveset (1993) of four species of chalcoid wasps predating seeds of Pistacia terebinthus.

Not preventing fruit maturation, as occurs with Revena spp. and Syagrw spp. (Bondar 1943, Guix and Ruiz 1995), may be an exaptation derived from the fact that larvae which survive interactions with frugivores are no longer selected to avoid encounters with them. For example, when frugivores normally kill insects contained in fruits, larvae may leave them before ripening (Herrera 1984), or, alternatively, may avoid ingestion by frugivores by inhibiting fruit maturation or otherwise reduce fruit quality (Kris- chick et al. 1989). Although probably not driven by natural selection, allowing fruit maturation may furnish advantages for both the seed-predator and the legitimate disperser. The frugivore has more re- sources available (mature fruits). The larva could be more effectively dispersed and benefit from escape from their own predators (Janzen 1970), as hypothesized for R. rubiginosa (Guix & Ruiz 1995). Since Syagrw seeds have only one locule, and the larva always kills a parasitized seed, the plant looses its reproductive investment in all cases when seeds are parasitized.

We do not know the extent to which baridine weevils rely on frugivores for dispersal. Since they have winged adult forms, at first glance they are able to disperse themselves (M.V.A. Alonso Zarazaga, pers. comm.). However, Bondar (1943) remarks that Revena spp. adults climb palm trees to reach fruits and reports never having observed an adult flying. In this case, the dispersal of Revena larvae by frugivores might constitute a highly relevant factor in this beetle’s life-history strategy.

We are grateful to Drs. Anna Traveset, Pedro Jordano, Woodruff W. Benson, and an anonymous referee for comments and criticism on earlier drafts of this paper, and to Dr. Lluis Jover for statistical advice. The late Dr. Werner C.A. Bokermann, Fundaglo Parque Zool6gico de Slo Paulo, provides help in conducting the feeding trials, and the Fundagso Florestal (Parque Estadual Intervales) and CEPARNIC (Parque Estadual Ilha do Cardoso) furnished logistic support during observational work on guans. Robin Rycroft (EIM, Universitat de Barcelona) improved the English text. Partial funding for this study was provided by the University of Barcelona through a travel grant to JCG. BONDAR, G. 1943. Notas entomolirgicas da Baia XlII. Rev. Entomol., Rio de Janeiro 14: 337-388. CHUNC, J. C., AND D. M. WALLER. 1986. Patterns of insect predation on seeds of smooth sumac (Rhus glabra L.).

Guix, J. C., AND X. Ruiz. 1995. Toucans and thrushes as potentid dispersers of seed-predatory weevil larvae in h e r . Midl. Nat. 116: 315-322.

Southeastern Brazil. Can. J. Zool. 73: 745-748.

Notes 525

HERRERA, C. M. 1982. Defense of ripe fruit from pests: its significance in relation to plant-disperser interactions. Am. Nat. 120: 219-241. . 1984. Avian interference of insect frugivory: an exploration into plant-bird-fruit pest evolutionary triad. Oikos 42: 203-210.

. 1977. Why fruits rot, seeds mold, and meat spoils. Am. Nat. 111: 691-713.

birds. Oikos 55: 375-386.

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berries infested with a cecidomyiid fly (Diptera: Cecidomyiidae). Am. Midl. Nat. 121: 350-354.

202.

Entomol. 37: 377-400.

cardiaceae). Vegetatio 107/108: 191-203.

JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104: 501-528.

JORDANO, I? 1989. Pre-dispersal biology of Pistaria fenriscw (Anacardiaceae): cumulative effects on seed removal by

KENWARD, R. 1987. Wildlife Radio Tagging: Equipment, Field Techniques and Data Analysis. Academic Press.

KFUSCHIK, V., E. S. MCCLOUD, AND J. A. DAVIDSON. 1989. Selective avoidance by vertebrate frugivores of green holly

NALEPA, C. A,, AND W. H. PIPER. 1994. Bird dispersal of the larval stage of a seed predator. Oecologia 100: 200-

SALLABANKS, R., AND S. I? C o u w N w . 1992. Frugivory, seed predation, and insect-vertebrate interactions. Annu. Rev.

TRAVESET, A. 1993. Weak interactions between avian and insect frugivores: the case of Pisruciu terrbinthus L. (Ana-

ZAR, J. H. 1984. Biostatistical Analysis. 2nd. Ed. Prentice Hall International. New Jersey.

Juan Carlos Guix and Xavier RuiP Departament de Biologia Animal (Vertebrats) Facultat de Biologia Universitat de Barcelona Avinguda Diagonal 645 E-08028 Barcelona Spain

To whom correspondence should be addressed.

BlOTROPlCA 29(4): 525-529 1997

The Effect of Lunar Illumination on Movement and Activity of the Red Fig-eating Bat (Sfenodema rufum)l Kqy word: radio telemetry

Chiroptera; ecology; lunar phobia; Luquillo Experimental Forest; Phyllostornidae; Puerto Rico;

MOONLIGHT is an environmental variable which depresses nocturnal activity in animals including insects (Williams & Singh 1951), rodents (Clarke 1983, Kotler 1984), and birds (Nelson 1989, Brigham & Barclay 1992). Moonlight also has been reported to reduce activity in bats by causing them to emerge later, or to restrict their flight and feeding to shadows (Reith 1982, Jones & Rydell 1994). Among the New World phyllostomids, Artibeus jamaicensis (Morrison 1975) and Desmodw rotundw (Crespo et al. 1972) significantly reduce activity during periods of high lunar illumination. This behavior, termed lunar phobia (Morrison 1978), suggests that flying in moonlight may significantly increase risk of predation by visually oriented predators. Predation pressure is a probable cause of this behavior because neither resource abundance and distribution, nor social activity in bats, is correlated with lunar illumination (Morrison 1978). Reduction in activity during periods of high lunar illumination is assumed to hold true for many other bat species (Erkert 1988).

Using radio telemetry, we examined the effects of lunar illumination on the movement patterns of the red fig-eating bat, Stenoderma nrfim, on Puerto Rico (Greater Antilles). In general, we evaluated differences in a variety of movement and activity parameters, the extent to which these parameters are

I Received 8 November 1995; revision accepted 15 April 1996.