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For Peer Review Only BIOTROPICA The relative contribut ion of specialists and generalists to mistletoe dispersal: insights from a Neotropical rainforest For Peer Review Only Journal: Biotropica Manuscript ID: BITR-11-411.R1 Manuscript Type: Paper Date Submitted by the Author: n/a Complete List of Authors: Watson, David; Charles Sturt University, The Johnstone Centre Barro Colorado Island, Frugivory and seed dispersal, Loranthaceae, Keywords: Tyrannidae, Foraging, Mionectes oleagineus, Miozetetes, Tyrannulus elatus, Zimmerius vilissimus Association for Tropical Biology and Conservation Page 1 of 34 BIOTROPICA 1 2 3 4 5 1 The relative contribution of specialists and generalists to mistletoe 6 7 8 2 dispersal: insights from a Neotropical rainforest 9 10 11 12 3 13 14 For Peer Review Only 15 4 DAVID M WATSON 16 17 18 5 Institute for Land Water and Society and School of Environmental Sciences 19 20 21 22 6 Charles Sturt University 23 24 25 7 PO Box 789 Albury 2640 Australia 26 27 28 8 29 30 31 9 Email [email protected] 32 33 34 10 35 36 37 38 11 Submitted as a standard paper to Biotropica 22 November 2011 39 40 41 12 Fully revised manuscript submitted 01 March 2012 42 43 44 13 45 46 47 14 Running head: Specialist vs generalist mistletoe dispersers 48 49 50 51 15 52 53 54 16 Received ____________; revision accepted ____________. 55 56 57 58 59 60 Association for Tropical Biology and Conservation BIOTROPICA Page 2 of 34 1 1 2 3 4 5 1 ABSTRACT 6 7 8 2 Mistletoes rely on birds for seed dispersal, but the presumed importance of mistletoe-specialist 9 10 3 frugivores has not been critically examined nor compared with generalist frugivores and 11 12 13 4 opportunistic foragers. The contribution of these three groups was compared directly by 14 For Peer Review Only 15 5 quantifying bird visitation to fruiting mistletoe plants ( Oryctanthus occidentalis : Loranthaceae) 16 17 6 at Barro Colorado Island, Panama, and by comparing these results with proportions calculated 18 19 20 7 from other empirical studies of mistletoe visitation conducted elsewhere. After more than 100 21 22 8 hours of timed watches, 23 bird species were recorded visiting eight heavily-infected host trees 23 24 9 (Luehea seemannii: Tiliaceae). Eight of these species visited mistletoe, of which five (all 25 26 27 10 tyrannids) consumed mistletoe fruit. Although two mistletoe specialist frugivores ( Tyrannulus 28 29 11 elatus and Zimmerius vilissimus ) removed most fruit (73%), more than a quarter was consumed 30 31 32 12 by one generalist frugivore ( Mionectes oleagineus ) and two opportunists ( Myiozetetes cayanensis 33 34 13 and Myiozetetes similis ). Post consumption behaviour varied: the specialists and generalist 35 36 14 frugivore flying from mistletoe to mistletoe, whereas the opportunists spent most time hawking 37 38 39 15 insects and resting high in the canopy. Integrating these data with previous work, the dietary 40 41 16 specialization, short gut passage rate and strict habitat preferences of mistletoe specialists 42 43 17 suggests that their services relate primarily to intensification and contagious dispersal, while 44 45 46 18 species with broader diets are more likely to visit uninfected trees and establish new infections. 47 48 19 The presumed importance of mistletoe-specialist frugivores was not supported and mistletoes are 49 50 considered to be comparable to many other bird-dispersed plants, relying on both specialist and 51 20 52 53 21 generalist frugivores, while opportunist may be disproportionately important in long-distance 54 55 22 dispersal. 56 57 58 59 60 Association for Tropical Biology and Conservation Page 3 of 34 BIOTROPICA 2 1 2 3 4 5 1 Key-words: Barro Colorado Island, Foraging, Frugivory and seed dispersal, Loranthaceae, 6 7 2 Mionectes oleagineus , Miozetetes , Tyrannulus elatus , Zimmerius vilissimus, Tyrannidae 8 9 10 3 11 12 13 14 For Peer Review Only 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Association for Tropical Biology and Conservation BIOTROPICA Page 4 of 34 3 1 2 3 4 5 1 Introduction 6 7 8 2 Many plants rely on animals as seed vectors, exhibiting various strategies to attract seed 9 10 3 dispersers and encourage their movement to favourable germination sites away from the parent 11 12 13 4 plant while minimizing losses from seed predators and other natural enemies. The relative 14 For Peer Review Only 15 5 contribution of seed dispersers to plant recruitment can be considered in terms of four factors— 16 17 6 frequency of visitation, number of seeds dispersed, quality of seed treatment and quality of seed 18 19 20 7 deposition—these interacting determinants known collectively as seed disperser effectiveness 21 22 8 (Schupp 1993, Schupp et al. 2010). This unifying concept emphasises between-disperser 23 24 9 differences and, although more inclusive than previous frameworks for studying endozoochorous 25 26 27 10 seed dispersal (Howe and Estabrook 1977, Wheelwright and Orians 1982), it is still limited by an 28 29 11 incomplete understanding of disperser movements (Rawsthorne et al. 2011a), the effects of seed 30 31 32 12 treatment on germinability (Restrepo and Martinez del Rio 1993) and the defining attributes of 33 34 13 safe sites for seedling establishment (Howe and Primack 1975). Even when these parameters are 35 36 14 known, variation in post-deposition factors—including seed predation, dormancy and secondary 37 38 39 15 dispersal—affect seed fate and eventual plant recruitment (Forget et al. 2002) making the 40 41 16 individual importance of a specific seed disperser to the recruitment of a specific plant difficult 42 43 17 to isolate and quantify. 44 45 46 47 18 Mistletoes are a diverse group of parasitic plants with a suite of life history characteristics 48 49 19 that makes them useful models to study seed dispersal: their seeds lack a testa and remain viable 50 51 20 for a matter of days, germination rates are high and independent of microclimate and safe sites 52 53 54 21 for establishment are readily defined by host range (Sargent 2000, Aukema and Martìnez del Rio 55 56 22 2004). Unlike most parasitic plants that attach to host roots below ground, mistletoes form 57 58 59 60 Association for Tropical Biology and Conservation Page 5 of 34 BIOTROPICA 4 1 2 3 4 5 1 permanent connections to the branches of their host (Mathiasen et al. 2008), a habit that makes 6 7 2 mistletoes more reliant on directed dispersal than any other group of plants (Restrepo et al . 2002, 8 9 3 Aukema 2004). Birds are the principal seed dispersers for most mistletoes, induced to transport 10 11 12 4 their sticky seeds by the surrounding parenchymatous pulp containing high fractions of 13 14 5 carbohydrates,For water, various Peer amino acids Review and fat (Watson 2001). Only Most research on mistletoe 15 16 17 6 seed dispersal has focused on mistletoe specialist frugivores, a group of birds from eight families 18 19 7 (Lybiidae, Tyrannidae, Cotingidae, Tityridae, Meliphagidae, Ptilogonatidae, Dicaeidae, 20 21 8 Fringillidae) that rely on mistletoe fruit as their principal food source (Davidar 1983, Godschalk 22 23 24 9 1985, Reid 1991, Watson 2001, Rawsthorne et al. 2011a). In addition to exhibiting behavioural 25 26 10 and anatomical adaptations to their restricted diet, many of these species feed mistletoe fruit to 27 28 11 their nestlings, making them some of the most specialized of all vertebrate frugivores (Snow 29 30 31 12 1981). 32 33 34 13 Although these dietary specialists may account for the majority of mistletoe fruits 35 36 14 consumed, their presumed importance as principal seed dispersers warrants further scrutiny. In 37 38 39 15 Europe, North Africa, Madagascar, New Zealand, most of North America and all oceanic 40 41 16 islands, mistletoe specialists are absent—mistletoe seeds are dispersed primarily by birds with 42 43 17 broad diets (Watson 2004, Mathiasen et al. 2008). Even in regions with mistletoe specialists, 44 45 46 18 many other birds consume mistletoe fruit and disperse their seeds (Reid 1989, López de Buen 47 48 19 and Ornelas 2001, Guerra and Marini 2002). Indeed, some of these non-specialists may be more 49 50 effective in dispersing seeds beyond existing infections, their broader diet necessitating regular 51 20 52 53 21 movement to stands and habitats without mistletoe and their longer gut passage rates allowing 54 55 22 longer-distance dispersal (Godschalk 1985, Rawsthorne et al. 2011a). So, if successful dispersal 56 57 58 23 is considered in terms of moving seeds to uninfected hosts (as in other host-parasite systems; 59 60 Association for Tropical Biology and Conservation BIOTROPICA Page 6 of 34 5 1 2 3 4 5 1 Boulinier et al. 2001), the services provided by specialists may actually be less effective than 6 7 2 birds with greater dietary breadth (Rawsthorne et al. 2011b). 8 9 10 3 Two landmark studies of mistletoe dispersal in the Neotropics compared proportions of 11 12 13 4 fruit consumed by specialist and non-specialist birds visiting different mistletoe species and 14 For Peer Review Only 15 5 considered components of dispersal services provided (Restrepo 1987, Sargent 1994; see also 16 17 6 Sargent 2000, Restrepo et al. 2002). By quantifying movement and perching preferences relative 18 19 20 7 to suitable sites for mistletoe establishment (at branch and tree scales), post-consumption 21 22 8 behaviour of specialists was demonstrated to lead to aggregation within already infected hosts 23 24 9 (Sargent 1994; see also Aukema 2004).
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