Integrative Zoology 2011; 6: 213-221 doi: 10.1111/j.1749-4877.2011.00245.x REVIEW Internal dispersal of seed-inhabiting insects by vertebrate frugivores: a review and prospects Ángel HERNÁNDEZ Department of Agroforestry, University of Valladolid, Palencia, Spain Abstract The finding that some seed-inhabiting insects can survive passage through the entire digestive tract of seed-dis- persing vertebrates is relatively recent, but evidence suggests that it does occur. Here, I document this phenomenon, discuss its qualitative and quantitative dimensions, and offer suggestions for further research. The few documented cases that I review include plant species belonging to different families, with varied fleshy fruit types, number of seeds per fruit and seed size. The vertebrate frugivores involved include passerines that feed on relatively small fruits, and galliforms, and perissodactyls and primates that feed on larger fruits. The seed-inhabiting insects in- volved are the larvae of seed-infesting wasps, parasitoid wasps and seed-infesting beetles. The phenomenon has been verified in open, rural ecosystems in North America and Southern Europe, and in tropical and subtropical forests in South America. These varied scenarios suggest that the qualitative dimension of the phenomenon is considerably greater than known thus far. A simple method for detecting new events is proposed. However, re- search must also focus on the identity and biology of seed-feeding insects of wild fleshy fruits and their parasitoids. High survival rates of seed-inhabiting insects after vertebrate gut passage are predominant. This phenomenon generally appears to favor insect dispersal. Key words: digestion-resistant insects, endozoochory, frugivory, tetratrophic interactions, tritrophic interactions. INTRODUCTION frugivore triads, the plant benefits from defending itself from the insect that damages the seed or the whole fruit, In plant-disperser-fruit pest triads in general, a mul- and the seed is dispersed; the disperser benefits from eat- tiple interaction occurs among 3 organism types, a plant, ing the pulp of ripe fruits; and the insect benefits from a seed-dispersing vertebrate and a phytophagous insect consuming the fruit without being killed by the disperser. or a pathogen, with different evolutionary consequences Plants defend their ripe fruits from insects in different ways of varying intensity (Herrera 1984a; Buchholz & Levey (e.g. phenology of fruit ripening, secondary compounds) 1990; Traveset 1993a; Willson & Traveset 2000; Silvius (Herrera 1982; Traveset 1993b), and fruit-infesting insects 2005). More precisely, in fleshy fruit-disperser-insect follow a number of strategies to avoid being killed by dis- persers (e.g. abandoning the fruit before it ripens, pre- venting it from ripening, or altering its physical and chemi- cal properties to make it undesirable for frugivorous Correspondence: Ángel Hernández, Department of Agroforestry, vertebrates) (Herrera 1989; Krischik et al. 1989). University of Valladolid (Palencia Campus), Avenida de Madrid Insect fruit predators can adapt to developing and liv- 44, 34071 Palencia, Spain. ing inside a seed, thus remaining isolated and protected Email: [email protected] from the environment by the seed coat (see Herrera 1989). © 2011 ISZS, Blackwell Publishing and IOZ/CAS 213 Á. Hernández Therefore, these insects could be expected to survive pas- were then removed from the droppings and examined for sage through the digestive tract of seed-dispersing adult eclosion and emergence. Seeds were defecated 30–210 vertebrates. This peculiar phenomenon of phoresy has only min after feeding. A total of 180 seeds were recovered from recently been confirmed, but it has already been verified the total of 200 fed to the bird (90%). Survival rate was 53% in several plant, vertebrate and insect species in several for bird-ingested insects and 46% for controls (infested seeds ecosystems and continents (Nalepa & Piper 1994; Guix that did not pass through the bird gut). Therefore, bird in- & Ruiz 1997; Bravo & Zunino 1998; Olmos et al. 1999; gestion did not contribute to mortality. Bravo 2008; Hernández 2009a). A surprising case of an In a rural habitat in north-west Spain, Hernández (2009a) evolutionary tetrad in which a parasitoid of a seed-infest- collected common blackbird (Turdus merula Linnaeus, ing insect resists bird ingestion and gut passage can now 1758) and thrush (mainly song thrush Turdus philomelos also be added (Hernández & Falcó 2008). Brehm, 1831) droppings, and observed larval survival and In the present paper, passive internal dispersal of fruit- adult emergence of M. aculeatus from dog rose (Rosa canina inhabiting insects facilitated by endozoochorous seed dis- Linnaeus, 1753) seeds contained in the droppings. Gut pas- persal is reviewed, taking into consideration the biological, sage time in common blackbirds is usually 30 min, although ecological and evolutionary characteristics and implications some seeds can be retained for longer (see Traveset et al. of this interaction, and suggesting further research to increase 2008). Hernández (2009a) reports rose seed infestation rates our knowledge of the phenomenon. The passive internal of 4.9 and 5.0%, and wasp survival rates (emerged adults dispersal of aquatic invertebrates by migratory waterbirds plus live larvae inside the seed) of 89 and 87% in early and (e.g. Green & Sánchez 2006) and the dispersal of seed-in- late winter, respectively. However, adult emergence rate was festing insects by imperfect harvesting (e.g. weevil-infested noticeably lower in droppings collected in early winter (54%) acorns scatter-hoarded by corvids or rodents that eventually than late winter (87%). escape predation) (see Guix & Ruiz 2000) are not covered here, as they do not involve endozoochory. Palms, birds and beetles In a rainforest in south-east Brazil, Guix and Ruiz (1995) SUMMARIZED DESCRIPTION OF found Revena rubiginosa (Boheman, 1836) weevils infest- ing the fruit of the palm tree Syagrus romanzoffiana KNOWN CASES ([Chamisso] Glassman, 1968), and an unidentified weevil Table 1 summarizes known cases of seed-inhabiting in- infesting the fruit of a myrtaceous tree (Eugenia sp.). The sects surviving passage through the entire digestive tract of fruits of both trees were eaten by toucans (red-breasted vertebrate frugivores, and shows the plant, vertebrate and Ramphastos dicolorus Linnaeus, 1766 and channel-billed insect taxa involved, as well as the insect survival rates and Ramphastos vitellinus Lichtenstein, 1823 toucans) and those the biomes from which these systems are reported. of the palm also by rufous-bellied thrushes (Turdus rufiventris Vieillot, 1818), and weevil larvae survived pas- Roses, birds and wasps sage through bird stomachs inside the seeds. However, seeds The larvae of the wasp Megastigmus aculeatus were regurgitated and not defecated owing to their large size (Swederus, 1795), widely distributed in the Holarctic region, and, therefore, larvae did not pass through the entire diges- feed on the endosperm of Rosa spp. seeds (Syrett 1990; tive tract of the birds. Therefore, the time of exposure to Nalepa & Grissell 1993; Roques & Skrzypczy ska 2003; mechanical and chemical digestive agents was short (2–30 Bruun 2006). Female wasps oviposit a single larva per seed min). in young green hips in spring-summer, just after petal fall. The same authors verified the survival of R. rubiginosa The larvae develop until the seed has hardened and then larvae inside S. romanzoffiana seeds, passing through the typically overwinter in diapause; adults usually exit the seed entire gut of captive dusky-legged guans (Penelope obscura the following spring-summer (Nalepa 1989; Nalepa & Temminck, 1815) (Guix & Ruiz 1997). Defecated seeds were Grissell 1993; Amrine 2002). Nalepa and Piper (1994) dem- collected and checked for exiting larvae (Revena weevils onstrated that wasps emerged after passage through the gut emerge from fruit as larvae and pupate in the soil). Of the of a northern mockingbird (Mimus polyglottos Linnaeus, 120 fruits offered to birds, 87 (73%) were ingested and their 1758). In the experiment, a captive bird was given pseudo- seeds collected from droppings. Gut retention time was ap- hips filled with crushed banana and wasp-infested multi- proximately 6 h. Of the 87 defecated seeds, 78 (90%) had flora rose (Rosa multiflora Thunberg, 1784) seeds, which weevil larvae inside; survival rate was nearly 100%. 214 © 2011 ISZS, Blackwell Publishing and IOZ/CAS Internal insect dispersal by frugivores Known cases of seed-inhabiting insects surviving passage through the entire digestive tract frugivorous vertebrates, in chronological order Table 1 Table © 2011 ISZS, Blackwell Publishing and IOZ/CAS 215 Á. Hernández Palms, tapirs and beetles The 5 cocoons corresponded to the 3 previously mentioned adult braconids and another 2 that probably emerged in the In a primary forest in south-east Brazil, Olmos et al. (1999) field before the droppings were collected. showed that R. rubiginosa larvae inside S. romanzoffiana seeds survive passage through the lowland tapir (Tapirus terrestris Linnaeus, 1758) digestive system. Gut passage time SCOPE OF THE PHENOMENON AND was 2–3 days for a captive tapir. The authors examined 844 SUGGESTIONS FOR FURTHER and 1092 palm seeds from new and old dung piles, respectively. Of the 844 seeds from new dung piles, 183 RESEARCH (22%) were alive (intact endosperm), 561 (66%) contained weevil larvae and 100 (12%) were empty seeds displaying