Influence of host-plant sex and habitat on survivorship of insect galls within the geographical range of the host-plant
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1 Tropical Zoology ISSN: (Print) (Online) Journal homepage: Influence of host-plant sex and habitat on survivorship of insect galls within the geographical range of the host-plant H. Nt. Ribeiro-Mendes, E. S.A. Marques, I. M. Silva & G. W. Fernandes To cite this article: H. Nt. Ribeiro-Mendes, E. S.A. Marques, I. M. Silva & G. W. Fernandes (2002) Influence of host-plant sex and habitat on survivorship of insect galls within the geographical range of the host-plant, Tropical Zoology, 15:1, 5-15, DOI: / To link to this article: Published online: 30 Jul Submit your article to this journal Article views: 98 View related articles Citing articles: 1 View citing articles Full Terms & Conditions of access and use can be found at Download by: [ ] Date: 07 January 2017, At: 06:22
2 Tropical Zoology 15: 5-15, 2002 Influence of host-plant sex and habitat on survivorship of insect galls within the geographical range of the host-plant H.NT. RIBEIRO-MENDES, E.S.A. MARQUES, I.M. SILVA and G.W. FERNANDES 1 Ecologia Evolutiva de Herbívoros Tropicais/DBG, ICB/Universidade Federal de Minas Gerais, CP 486, Belo Horizonte, MG, Brazil Received 4 July 2000, accepted 16 March 2002 This study evaluated the influence of host-plant sex and habitat on the abundance and survivorship of the galling Psyllidae, Neopelma baccharidis Burckhardt 1987 (Homoptera) on several populations of the host-plant Baccharis dracunculifolia De Candole (Asteraceae) within its geographical range in Brazil. Three questions were addressed: (i) what is the effect of host-plant sex and the habitat occupied by Baccharis dracunculifolia on the abundance of galls induced by Neopelma baccharidis? Plant sex did not affect the abundance of galls per plant while host-plant habitat had a significant effect. Twice as many galls were found on plants in xeric habitats as on plants in mesic habitats; (ii) what is the influence of host-plant sex and habitat on the survivorship rates of Neopelma baccharidis? Populations occurring in mesic habitats suffered 3 times greater mortality than populations in xeric habitats; (iii) does the richness and abundance of inquilines of Neopelma baccharidis galls vary between habitats? Habitat type did not influence the pattern of inquiline richness. The abundance of inquilines was also very similar between xeric (51%) and mesic habitats (49%). This study suggests that host-plant sex did not affect the abundance of the psyllid galls on B. dracunculifolia, while the habitat occupied by the host-plant had a strong influence on gall abundance, with more galls occurring in xeric habitats than in mesic habitats. Otherwise, no effect of habitat was found on gall inquilines. The mechanism generating the pattern of gall abundance was the differential mortality of galls between habitat types. KEY WORDS: habitat effects, herbivory, insect galls, plant sex, richness, survivorship. Introduction Materials and methods Results and discussion Acknowledgements References Correspondence: G. Wilson Fernandes ( gwilson@icb.ufmg.br).
3 6 H.Nt. Ribeiro-Mendes et alii INTRODUCTION Host-plant quality and the habitat in which a plant grows influence several physiological attributes of the plants which in turn affect the ecological niche for their associated insect herbivores (ELMQVIST et al. 1991; FERNANDES & PRICE 1991, 1992; WATSON 1995). For instance, secondary compounds are affected by the nutritional status of the plant and habitat type, therefore exerting strong selective pressure on the establishment and success of herbivores (BRYANT et al. 1983, COLEY et al. 1985, HERMS & MATTSON 1992). Another source of variation is plant gender. The sex-mediated herbivory hypothesis predicts that male plants will be preferentially attacked by herbivores (e.g., BOECKLEN et al. 1990, HERMS & MATTSON 1992) because male plants allocate more energy into growth (biomass) while female plants allocate more energy into reproduction (e.g., ÅGREN 1988, POPP & REINARTZ 1988). This would result in qualitative and quantitative differences in defenses (see BRYANT et al. 1983, COLEY et al. 1985) and in nutritional deficiencies caused by the increased cost of reproduction in female plants. Reproductive costs are generally higher for female plants, resulting in nutrient deficiency when compared to male plants (FREEMAN et al. 1976, 1980; WILSON 1979; WHITHAM & MOPPER 1985; KRISCHIK & DENNO 1990). Environmental factors such as water and nutritional stress can alter growth rates and the C/N balance which causes changes in the type of chemical defenses employed by the host plants (BRYANT et al. 1983, COLEY et al. 1985, HORNER & ABRAHAMSON 1992), thereby resulting in differential herbivory rates and herbivore densities between plants (BOECKLEN et al. 1990, 1994; BOECKLEN & HOFF- MAN 1993). Galling insects have been widely used to test hypotheses on differential herbivory between habitats. Several studies have shown greater frequencies of attacked plants, gall densities and richness in xeric habitats than in mesic ones (FERNANDES & PRICE 1988, 1991; WARING & PRICE 1990; FERNANDES 1992; LARA & FERNANDES 1994). A previous study by FERNANDES & PRICE (1992), mostly conducted in the temperate region, showed that six out of eight galling species occurring on six species of host plants had greater abundances in xeric habitats. Populations of galling species in xeric habitats suffered lower mortality due to natural enemies and plant resistance than populations in mesic habitats. Therefore, the mechanism responsible for the occurrence of more gall species in xeric sites was the differential mortality and survivorship of galls between habitats. However, no such study has been performed in the tropical region or in more detail along the geographical distribution of a single host plant. Inquilines are another group of organisms that coexist in the triple trophic system of host-plants-galling herbivores-parasitoids. Often found inside galls associated with the live galling larvae, they seek refuge, protection and food (MANI 1964, FERNANDES et al. 1988, SUAREZ & CALVO 1989). We postulate that inquilines, like galling herbivores and parasitoids, should also be sensitive to changes in gall biology and habitat type. Nevertheless, the richness and abundance of gall inquilines has not yet been evaluated as a function of the habitat occupied by the host plants. This study evaluated the influence of host-plant sex and habitat type on the abundance and survivorship of the galling psyllid Neopelma baccharidis (Homoptera Psyllidae) and of its inquilines on Baccharis dracunculifolia De Candole (Asteraceae). The following questions were addressed: (i) what is the effect of the habitat and sex of B. dracunculifolia on the abundance of N. baccharidis galls?; (ii) what is the influence of host-plant sex and habitat on the survival rates of N. bac-
4 On insect gall survival 7 charidis?; (iii) do the richness and abundance of inquilines of N. baccharidis galls vary between habitats? Because ecological mechanisms can vary locally and geographically, we studied several populations of galls in the distributional range of the plant in Brazil, in an attempt to ascertain if the trends found varied across the host range and to account for the possible variations. MATERIALS AND METHODS System Baccharis dracunculifolia De Candole (Asteraceae) is a widespread dioecious perennial shrub, ranging in height from 2 to 3 m and occurring in southeastern and southern Brazil, Argentina, Paraguay, Uruguay and Bolivia (KISSMANN & GROTH 1992). It occurs in open habitats, such as natural fields or disturbed areas, forming dense homogeneous patches of vegetation. Neopelma baccharidis Burckhardt 1987 is the most common galling insect on B. dracunculifolia (ARAUJO et al. 1995). The leaf galls induced by N. baccharidis are elliptical, green, glabrous, one-chambered with several overlapping generations per year (ESPIRITO-SANTO & FERNANDES 1998). Females oviposit on the main vein of young leaves and the tissue becomes swollen, bending over itself until its borders join, thereby, forming an elliptical capsule (LARA & FERNANDES 1994). Gall walls are succulent throughout the development of the psyllid. Even after dehiscence and emergence of the adults, the gall remains adhered to the plant, undergoing gradual desiccation until it becomes dry and woody (LARA & FERNANDES 1994). N. baccharidis abundance varies throughout the year, being greater during the reproductive phases of the host-plant (ESPIRITO-SANTO & FERNANDES 1998). Study site Ten populations of B. dracunculifolia were collected in four different Brazilian states (Table 1). Five populations were located in mesic habitats (Atlantic rainforest) and the other Table 1. Habitat, location, geographical coordinates and biome of the populations of B. dracunculifolia studied. Habitat Location Geographical coordinates Biome Xeric Serra do Cipó (MG) S 44º20 W Cerrado Felixlândia (MG) 18º45 S 44º50 W Cerrado Perdizes (MG) 19º10 S 47º15 W Cerrado Confins (MG) 19º10 S 47º15 W Cerrado Ouro Branco (MG) 20º30 S 43º40 W Rupestrian field Mesic Caratinga (MG) 19º50 S 41º50 W Atlantic rainforest Canela (RS) 29º20 S 50º53 W Atlantic rainforest Poço das Antas (RJ) S 42 o 20 W Atlantic rainforest Curitiba (PR) S W Atlantic rainforest Ouro Preto (MG) 20º23 S 43º34 W Atlantic rainforest
5 8 H.Nt. Ribeiro-Mendes et alii five in xeric habitats (cerrado and rupestrian field). Cerrado is equivalent to a moist savanna with sub-tropical, moderately humid climate; although mean yearly precipitation varies from 200 to 1800 mm the strong dry season results in water deficits up to 60 mm (HUECK 1972). Mean annual temperatures oscillate between 17 and 25 C causing annual evapotranspiration potentials of 700 to 850 mm. Soils are well drained, dystrophic, with low ph and availability of calcium and magnesium, and high concentrations of aluminum (HUECK 1972, GONÇALVES- ALVIM & FERNANDES 2001). The rupestrian fields of Serra do Cipó are located in the cerrado domain; they share many of the same climatic characteristics but are limited to higher elevations where soils are nutrient-poor, acidic and rocky with poor water retention (FERNANDES 1994, RIBEIRO & FERNANDES 2000). The Atlantic rainforest domain is represented by several different vegetation types ranging from tropical humid forests to subtropical seasonal semideciduous forests. Precipitation ranges from 1700 to 3600 mm a year with mild temperatures throughout the year (17 to 25 o C) and 88% relative humidity (HUECK 1972). Methods To determine whether xeric habitats showed a greater abundance of galls than mesic habitats and whether male plants supported more galls than female plants we randomly sampled 50 individuals of B. dracunculifolia in each population (25 male and 25 female plants) (see ARAUJO et al. 1995, SILVA et al. submitted). All shoots on the plants were cut at stem level, placed in labeled plastic bags, and then taken to the laboratory where all N. baccharidis galls were counted. Gall abundance per plant was compared between habitats and plant sex by the Mann-Whitney test, since the data did not show normal distribution (ZAR 1974). Differential survival between habitats and plant sex was inferred from data on nymph mortality of N. baccharidis from the previous generation (green and succulent galls) (ESPIRITO- SANTO & FERNANDES 1998). Gall mortality factors were separated into parasitism, predation, fungi, plant resistance, and unknown factors based on criteria adopted by FERNANDES & PRICE (1992): parasitism = when parasitoid exuviae remained inside the gall and/or the presence of parasitoid exit holes; plant resistance = when gall tissue was necrotic, or when the gall chamber was obliterated by the growth of gall tissue, crushing the gall nymphs; predation = when any external signs of perforation or chewing of the gall walls were observed or the galler had been preyed upon, resulting in missing body parts; fungi = when the gall chamber was filled by fungi; other = this category included galls in which the nymph was found dead but the causes of death were unclear. To address whether inquiline richness and abundance in galls of N. baccharidis varied between habitats, all arthropods found inside the galls were counted and separated into morphospecies. These data were analyzed by the Mann-Whitney test, as they were not normally distributed (ZAR 1974). RESULTS AND DISCUSSION The number of N. baccharidis galls per plant was highly variable among the populations studied. Male plants did not support more galls than female plants in any of the 10 populations studied (Mann-Whitney U = 31996, n = 500, P > 0.05). The mean number of galls on male plants was 9.03 ± 1.31 (± 1 SE), while female plants had a mean of 5.57 ± 0.72 (± 1 SE) galls per plant. When the mean numbers of galls per sex were compared in each population, more galls were found on male plants only in Perdizes, MG (Table 2). The present study is among five others in the neotropics that have not corroborated the sex-mediated herbivory hypothesis (MADEIRA et al. 1997, ESPIRITO-SANTO & FERNANDES 1998, FARIA & FERNANDES 2001,
6 On insect gall survival 9 Table 2. Mean number of galls on male and female plants of 10 populations of B. dracunculifolia. Comparisons performed with the U-test (P > 0.05, all). Location Habitat Mean number of galls Male Female U-test Poço das Antas mesic 1.84 ± ± Caratinga mesic 6.52 ± ± Canelas mesic 2.44 ± ± Ouro Preto mesic 6.64 ± ± Curitiba mesic 2.36 ± ± Confins xeric ± ± Felixlândia xeric ± ± Serra do Cipó xeric 5.56 ± ± Perdizes xeric ± ± Ouro Branco xeric 2.88 ± ± MARQUES et al. in press, SILVA et al. submitted). Since plant sex did not affect gall abundance the data were pooled in the remaining analyses. The sex-mediated herbivory hypothesis is based upon differential growth between the sexes, resulting in differences in the quality and types of defenses utilized by the host-plant (BRYANT et al. 1983, COLEY et al. 1985) and in nutritional deficiencies caused by the increased cost of reproduction in female plants. It is possible that B. dracunculifolia does not exhibit significant differences in growth rates or nutritional status between male and female plants. If so, differences in the types or quality of defenses between plant sexes would not be observed. Future studies will evaluate the nutritional quality of male and female B. dracunculifolia plants to further test this hypothesis. Host-plant habitat strongly affected gall abundance per plant (Mann-Whitney U = , n = 500, P < 0.05). Twice the number of galls were found on plants in xeric habitats than on plants in mesic habitats. The mean number of galls per plant in xeric habitats was ± 1.51 (± 1 SE) while the mean number of galls in mesic habitats was only 7.7 ± 1.16 (± 1 SE) galls per plant. These results, from different populations along the geographical range of the host plant, support earlier studies of local populations where different plant species supported greater abundances of galling insects at xeric sites than that mesic sites (FERNANDES & PRICE 1992). Furthermore, as this study covered 10 populations in four states of Brazil (range of 18-29º latitude south), it suggests that the pattern of greater survival of galls in xeric habitats, which until now had only been documented at a local scale, also occurs at a regional scale. In total, 5,574 galls were found on the 500 individuals in the 10 populations studied. Of these, 3,649 galls were dissected to evaluate N. baccharidis mortality factors. Populations occurring on plants in similar habitats were grouped as a function of the survival rates of N. baccharidis in a hierarchical cluster analysis using Euclidean distances (Fig. 1) (WILKINSON et al. 1998). Mortality of N. baccharidis in mesic habitats (6.07 ± 1.18%) was almost 3 times greater than in xeric habitats (2.22 ± 1.22%). The factors that contributed most to gall mortality was parasitism
7 10 H.Nt. Ribeiro-Mendes et alii Minimum connection Fig. 1. Cluster analysis of mean gall survival per plant in 10 different populations of Baccharis dracunculifolia sampled in Brazil. Perdizes (Perd), Serra do Cipó (Cipó), Confins (Conf), Felixlândia (Felix) in xeric habitats; Canela (Cane), Poço das Antas (Anta), Caratinga (Cara), Ouro Preto (Pret), Curitiba (Curi) in mesic habitats, while the population of Ouro Branco (Bran) differed from the others. by microhymenopteran wasps (68.01 ± 1.94%): 87% of the wasp-parasitized galls were attacked by one parasitoid morphospecies out of six species encountered. Among all mortality factors acting upon N. baccharidis, predation (Mann-Whitney U = 7,474, n = 266, P < 0.005) and parasitism (Mann-Whitney U = 6,770.5, n = 266, P < 0.001) showed significant differences between habitats. The other mortality factors were not influenced by habitat type (fungi: Mann-Whitney U = 8,460.5, n = 266, P > 0.597; plant resistance: Mann-Whitney = 8,661.5, n = 266, P > 0.906; other: Mann-Whitney U = 8,614.5, n = 266, P > 0.861; Fig. 2). Therefore, gall survivorship was higher in xeric habitats than in mesic habitats. N. baccharidis survival was related to habitat type. Populations from similar habitat types showed similar mean gall survival rates per plant, except for two populations, one in a xeric habitat in Ouro Branco (Bran) and the other in a mesic habitat in Canela (Cane). The Ouro Branco population (rupestrian field vegetation) showed the lowest survival rates and stood alone, differing from both mesic and xeric sites. This exception was probably due to the fact that the Ouro Branco population was located next to gallery forest vegetation (< 10 m), where soils are richer in nutrients and deeper, enabling greater water retention (Fig. 1). The Canela population
8 On insect gall survival Parasitism (%) Female Male Fungi (%) Predation (%) Plant Resistance (%) Others (%) Poço das Antas Caratinga Canela Curitiba Ouro Preto Confins Felixlândia Serra do Cipó Perdizes Ouro Branco Fig. 2. Mortality rates of Neopelma baccharidis, between habitats and host-plant sex, in 10 populations of Baccharis dracunculifolia. Perdizes (Perd), Serra do Cipó (Cipó), Confins (Conf), Felixlândia (Felix) in xeric habitats; Canela (Cane), Poço das Antas (Anta), Caratinga (Cara), Ouro Preto (Pret), Curitiba (Curi) in mesic habitats.
9 12 H.Nt. Ribeiro-Mendes et alii (Atlantic rainforest), on other hand, showed higher survival rates than the other mesic sites and was grouped with the xeric sites. This was probably due to the fact that this population belonged to a seasonal semi-deciduous forest which is typically less humid than the other vegetational types in Atlantic rainforests (HUECK 1972). FERNANDES & PRICE (1992) used the harsh environment hypothesis to explain the greater abundances and survival rates of galls in xeric habitats. This hypothesis predicts that in xeric habitats, with diminished availability of water and nutrients, the pressure caused by natural enemies and plant resistance would be lower than in humid habitats (mesic habitats). Plants in mesic habitats would then be better defended against gallers than those occurring in xeric habitats (see FERNANDES 1990, 1998) and gallers would also suffer lower pressure by parasites and predators. Accordingly, only mortality rates caused by predation and parasitism were statistically different between habitats, being higher in mesic than in xeric habitats. In total, 104 individual inquilines were found in the 3,649 galls dissected. Inquiline abundance did not differ statistically between xeric habitats (51%) and mesic habitats (49%) (Table 3). Thirteen inquiline morphospecies were found in this study (Table 3). Contrary to SUAREZ & CALVO (1989) and FERNANDES et al. (1989), inquilinism was a rare event in Neopelma baccharidis galls: all the inquilines present (104) were found in only 1.9% of the galls sampled. The high overall abundance of inquilines in the few utilized galls was due to the high frequency of thrips in some galls. Thrips sp. 1 (Thysanoptera), acari, aphid sp. 1 and aphid sp. 2 were present in both habitats with similar frequencies. Aphid sp. 1 and sp. 2 were more frequent in xeric habitats, while dipteran sp. 1 was more frequent Table 3. Total inquiline richness and abundance and diversity indexes in galls of Neopelma baccharidis in mesic and xeric habitats. Morphospecies Xeric Habitat Mesic 1. Thrips sp Aphidoidea sp Diptera sp Aphidoidea sp Cecidomyiidae sp Lepidoptera sp Acari sp Lepdoptera sp Coleoptera sp Coccoidea sp Aphidoidea sp Mite sp. 2 1 Total abundance Richness 9 7 Pielou J (Evenness) H (Diversity) Morisita-Horn 0.893
10 On insect gall survival 13 in mesic habitats (Table 3). Of the morphospecies occurring in xeric habitats, five were restricted to this habitat type (Cecidomyiidae, Lepidoptera sp. 2, Coleoptera sp. 1, Coccoidea sp. 1, Aphidoidea sp. 3). Except for Lepidoptera sp. 2 (four occurrences), all other species had only one occurrence. There were three morphospecies (Coleoptera sp. 1, Coccoidea sp. 1, Aphidoidea sp. 3) that only occurred in mesic habitats but had only one occurrence. Inquiline diversity (three indexes evaluated) did not differ between habitat type, while there appeared to be different inquiline faunas in the different habitats (Table 3). Future studies at broader scales are needed, however, to unveil the biology of inquilines in N. baccharidis galls in different habitat types. ACKNOWLEDGEMENTS We thank W.G. Abrahamson and two anonymous reviewers for their helpful suggestions on the manuscript and W. de Andrade for field and laboratory assistance. This project was supported by Fapemig (CBS 2519/97), CNPq ( /95-8) and International Foundation for Science H/ REFERENCES ÅGREN J Sexual differences in biomass and nutrient allocation in the dioecious Rubus chamemorus. Ecology 69: ARAUJO A.M., FERNANDES G.W. & BEDE L.C Influência do sexo e fenologia de Baccharis dracunculifolia DC (Asteraceae) sobre insetos herbívoros. Revista Brasileira de Entomologia 39: BOECKLEN W.J. & HOFFMAN M.T Sex-biased herbivory in Ephedra trifurca: the importance of sex-by-environment interactions. Oecologia 93: BOECKLEN W.J., MOPPER S. & PRICE P.W Sex-biased herbivory in arroyo willow: are there general patterns among herbivores? Oikos 71: BOECKLEN W.J., PRICE P.W. & MOPPER S Sex and drugs and herbivores: sex-biased herbivory in arroyo willow (Salix lasiolepsis). Ecology 71: BRYANT J.P., CHAPIN F.S. & KLEIN D.R Carbon/nutrient balance in boreal plants in relation to vertebrate herbivory. Oikos 40: COLEY P.D., BRYANT J.P. & CHAPIN III F.S Resource availability and plant antiherbivore defense. Science 230: ELMQVIST T., CATES R.G., HARPER J.K. & GARDFJELL H Flowering in males and females of a Utah willow, Salix rigida, and effects on growth, tannins, phenolic glycosides and sugars. Oikos 61: ESPIRITO-SANTO M.M. & FERNANDES G.W Abundance of Neopelma baccharidis (Homoptera: Psyllidae) galls on the dioecious shurb Baccharis dracunculifolia (Asteraceae). Environmental Entomology 27: FARIA M.L. & FERNANDES G.W Vigour of a dioecious shrub and attack by a galling herbivore. Ecological Entomology 26: FERNANDES G.W Hypersensitivity: a neglected plant resistance mechanism against insect herbivores. Environmental Entomology 19: FERNANDES G.W Adaptive distribution of gall-forming insects: patterns and mechanisms. Unpublished PhD Dissertation, Northern Arizona University, Flagstaff, Arizona, 99 pp. FERNANDES G.W Plano de ação emergencial do Parque Nacional da Serra do Cipó. Brasília D.F.: IBAMA, 177 pp.
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