Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation.

Urbanization within the Tucson Basin of Arizona during the past 50+ years has fragmented the original desert scrub into patches of different sizes and ages. These remnant patches and the surrounding desert are dominated by Larrea tridentata (creosote bush), a long-lived shrub whose flowers are visited by > 120 native bee species across its range. Twenty-one of these bee species restrict their pollen foraging to L. tridentata. To evaluate the response of this bee fauna to fragmentation, we compared species incidence and abundance patterns for the bee guild visiting L. tridentata at 59 habitat fragments of known size (0.002-5 ha) and age (up to 70 years), and in adjacent desert. The 62 bee species caught during this study responded to fragmentation heterogeneously and not in direct relation to their abundance or incidence in undisturbed desert. Few species found outside the city were entirely absent from urban fragments. Species of ground-nesting L. tridentata specialists were underrepresented in smaller fragments and less abundant in the smaller and older fragments. In contrast, cavity-nesting bees (including one L. tridentata specialist) were overrepresented in the habitat fragments, probably due to enhanced nesting opportunities available in the urban matrix. Small-bodied bee species were no more likely than larger bodied species to be absent from the smaller fragments. The introduced European honey bee, Apis mellifera, was a minor faunal element at > 90% of the fragments and exerted little if any influence on the response of native bee species to fragmentation. Overall, bee response to urban habitat fragmentation was best predicted by ecological traits associated with nesting and dietary breadth. Had species been treated as individual units in the analyses, or pooled together into one analysis, these response patterns may not have been apparent. Pollination interactions with this floral host are probably not adversely affected in this system because of its longevity and ability to attract diverse pollinators but will demand careful further study to understand.

[1]  T. Tscharntke,et al.  Trap-nesting bees and wasps colonizing set-aside fields: succession and body size, management by cutting and sowing , 1994, Oecologia.

[2]  J. C. Marlin,et al.  The Native Bee Fauna of Carlinville, Illinois, Revisited After 75 Years: a Case for Persistence , 2001 .

[3]  Marcelo A. Aizen,et al.  Forest Fragmentation, Pollination, and Plant Reproduction in a Chaco Dry Forest, Argentina , 1994 .

[4]  B. D. Burks,et al.  Catalog of Hymenoptera in America north of Mexico. Volume 1. Symphyta and Apocrita (Parasitica). , 1981 .

[5]  James H. Brown,et al.  Highly structured fish communities in Australian desert springs , 1993 .

[6]  C. Michener The Bees of the World , 2000 .

[7]  E. Linsley The ecology of solitary bees , 1958 .

[8]  J. Cane The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields , 1997 .

[9]  John H. Lawton,et al.  BEETLE SPECIES RESPONSES TO TROPICAL FOREST FRAGMENTATION , 1998 .

[10]  Diego P. Vázquez,et al.  Changes in interaction biodiversity induced by an introduced ungulate , 2003 .

[11]  S. Trueman,et al.  Clonality and sexual reproductive failure in remnant populations of Santalum lanceolatum (Santalaceae) , 2000 .

[12]  P. Gouyon,et al.  THE ECOLOGICAL CONSEQUENCES OF FLOWERING ASYNCHRONY IN MONOECIOUS FIGS: A SIMULATION STUDY' , 1990 .

[13]  Paul D. Allison,et al.  Logistic Regression Using the SAS System : Theory and Application , 1999 .

[14]  T. Tscharntke,et al.  How does landscape context contribute to effects of habitat fragmentation on diversity and population density of butterflies? , 2003 .

[15]  S. Herzog,et al.  SEASONAL VARIATION IN AVIAN COMMUNITY COMPOSITION IN A HIGH-ANDEAN POLYLEPIS (ROSACEAE)FOREST FRAGMENT , 2003 .

[16]  V. Kaitala,et al.  Predicting the risk of extinction from shared ecological characteristics. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[17]  David Tilman,et al.  Human-caused environmental change: Impacts on plant diversity and evolution , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  T. Tscharntke,et al.  Habitat Fragmentation, Species Loss, and Biological Control , 1994, Science.

[19]  J. Cane,et al.  Spatial predictability and resource specialization of bees (Hymenoptera: Apoidea) at a superabundant, widespread resource , 1999 .

[20]  J. Cane,et al.  Temporally persistent patterns of incidence and abundance in a pollinator guild at annual and decadal scales: the bees of Larrea tridentata , 2005 .

[21]  P. Poschlod,et al.  Genetical Aspects of Fragmented Plant Populations , 1996 .

[22]  J. Cane Exotic non-social bees (Hymenoptera: Apoidea) in North America: Ecological implications , 2003 .

[23]  Ola Jennersten Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set , 1988 .

[24]  Robert H. Webb,et al.  Succession of desert plants on debris flow terraces, Grand Canyon, Arizona, U.S.A. , 1997 .

[25]  R. Dressler BIOLOGY OF THE ORCHID BEES (EUGLOSSINI) , 1982 .

[26]  R. Macarthur,et al.  The Theory of Island Biogeography , 1969 .

[27]  Glenn D. Sutherland,et al.  Scaling of Natal Dispersal Distances in Terrestrial Birds and Mammals , 2000 .

[28]  R. Frankl,et al.  Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., Apidae), in an agricultural landscape , 2000 .

[29]  V. Tepedino,et al.  Reproductive biology of the rare orchid, Spiranthes diluvialis: Breeding system, pollination, and implications for conservation , 1995 .

[30]  J. Cane Nesting resins obtained from pollen host by an oligolectic bee, Trachusa larreae (Cockerell) (Hymenoptera: Megachilidae) , 1996 .

[31]  M. Ohara,et al.  Genetic diversity and local population structure of fragmented populations of Trillium camschatcense (Trilliaceae) , 2003 .

[32]  Marie-Charlotte Anstett,et al.  Modeling the Persistence of Small Populations of Strongly Interdependent Species: Figs and Fig Wasps , 1997 .

[33]  T. Ricketts The Matrix Matters: Effective Isolation in Fragmented Landscapes , 2001, The American Naturalist.

[34]  Robert M. May,et al.  Dynamics of metapopulations : habitat destruction and competitive coexistence , 1992 .

[35]  Wirt Atmar,et al.  The measure of order and disorder in the distribution of species in fragmented habitat , 1993, Oecologia.

[36]  C. Schultz,et al.  Dispersal Behavior and Its Implications for Reserve Design in a Rare Oregon Butterfly , 1998 .

[37]  A. Joern,et al.  LANDSCAPE VS. LOCAL HABITAT SCALE INFLUENCES TO INSECT COMMUNITIES FROM TALLGRASS PRAIRIE REMNANTS , 2004 .

[38]  Douglas T. Bolger,et al.  Reconstructed Dynamics of Rapid Extinctions of Chaparral‐Requiring Birds in Urban Habitat Islands , 1988 .

[39]  D. H. Boshier,et al.  Increased pollen flow counteracts fragmentation in a tropical dry forest: An example from Swietenia humilis Zuccarini , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  C. Michener,et al.  Factors Influencing the Distribution of Bees' Nests in Earth Banks , 1958 .

[41]  I. Washitani Predicted genetic consequences of strong fertility selection due to pollinator loss in an isolated population of Primula sieboldii , 1996 .

[42]  E. Menges Seed Germination Percentage Increases with Population Size in a Fragmented Prairie Species , 1991 .

[43]  Gretchen C Daily,et al.  Economic value of tropical forest to coffee production. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  P. J. Boer The significance of Dispersal Power for the Survival of Species, with Special Reference to the Carabid Beetles in a Cultivated Countryside , 1979 .

[45]  Elizabeth E. Crone,et al.  EDGE-MEDIATED DISPERSAL BEHAVIOR IN A PRAIRIE BUTTERFLY , 2001 .

[46]  R. Turner Long‐Term Vegetation Change at a Fully Protected Sonoran Desert Site , 1990 .

[47]  S. Kalinowski,et al.  INBREEDING DEPRESSION IN CONSERVATION BIOLOGY , 2000 .

[48]  F. R. Cole,et al.  Effects of the Argentine Ant on Arthropod Fauna of Hawaiian High‐Elevation Shrubland , 1992 .

[49]  M. Holyoak,et al.  Riparian habitat fragmentation and population persistence of the threatened valley elderberry longhorn beetle in central California , 2001 .

[50]  T. Tscharntke,et al.  Effects of habitat isolation on pollinator communities and seed set , 1999, Oecologia.

[51]  Tom J. Mabry,et al.  Creosote bush. Biology and chemistry of Larrea in New World deserts. , 1978 .

[52]  P. Hedrick,et al.  Testing for inbreeding and outbreeding depression in the endangered Gila topminnow , 1999 .

[53]  R. G. Davies Feeding group responses of a Neotropical termite assemblage to rain forest fragmentation , 2002, Oecologia.

[54]  David W. Inouye,et al.  ENDANGERED MUTUALISMS: The Conservation of Plant-Pollinator Interactions , 1998 .

[55]  E. Fernández-Juricic Spatial and temporal analysis of the distribution of forest specialists in an urban-fragmented landscape (Madrid, Spain) Implications for local and regional bird conservation , 2004 .

[56]  A. Love The Evolution of Flowering Plants , 1975, The Quarterly Review of Biology.

[57]  Jean Clobert,et al.  Influence of connectivity on demography and dispersal in two contrasting habitats: an experimental approach , 1999 .

[58]  Christopher W. Dick Genetic rescue of remnant tropical trees by an alien pollinator , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[59]  Dennis D. Murphy,et al.  Conservation Strategy: The Effects of Fragmentation on Extinction , 1985, The American Naturalist.

[60]  B. Rathcke,et al.  Habitat fragmentation and plant-pollinator interactions , 1993 .

[61]  C. Margules,et al.  A SYNERGISTIC EFFECT PUTS RARE, SPECIALIZED SPECIES AT GREATER RISK OF EXTINCTION , 2004 .

[62]  P. Stouffer,et al.  Effects of Forest Fragmentation on Understory Hummingbirds in Amazonian Brazil. , 1995, Conservation biology : the journal of the Society for Conservation Biology.

[63]  P. D. Hurd,et al.  The principal Larrea bees of the southwestern United States (Hymenoptera: Apoidea) , 1975 .

[64]  J. Cane Estimation of bee size using intertegular span (Apoidea) , 1987 .

[65]  J. Cane,et al.  Biological impediments to measures of competition among introduced honey bees and desert bees , 2003 .

[66]  J. Neff,et al.  Foraging and nesting biology of the bee Anthemurgus passiflorae (Hymenoptera, Apoidea), descriptions of its immature stages, and observations on its floral host (Passifloraceae). American Museum novitates ; no. 3138 , 1995 .

[67]  Neal M. Williams,et al.  Crop pollination from native bees at risk from agricultural intensification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[68]  S. Porter,et al.  Invasion of Polygyne Fire Ants Decimates Native Ants and Disrupts Arthropod Community , 1990 .

[69]  V. B. Huryn Ecological Impacts of Introduced Honey Bees , 1997, The Quarterly Review of Biology.

[70]  J. Cane Soils of ground-nesting bees (Hymneoptera: Apoidea): Texture, moisture, cell depth and climate , 1991 .

[71]  D. Bonte,et al.  Effects of aerial dispersal, habitat specialisation, and landscape structure on spider distribution across fragmented grey dunes , 2004 .

[72]  T. Burgess,et al.  Sonoran Desert Plants: An Ecological Atlas , 1995 .

[73]  I. Turner Species loss in fragments of tropical rain forest: a review of the evidence. , 1996 .

[74]  J. Cane Habitat Fragmentation and Native Bees: a Premature Verdict? , 2001 .

[75]  J. Cane,et al.  Origins and ecological consequences of pollen specialization among desert bees , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[76]  E. Fernández-Juricic Nested patterns of species distribution and winter flock occurrence of insectivorous birds in a fragmented landscape , 2002 .

[77]  C. Christian Consequences of a biological invasion reveal the importance of mutualism for plant communities , 2001, Nature.

[78]  Phil Rau,et al.  Experimental studies in the homing of carpenter and mining bees , 1929 .

[79]  M. Soulé,et al.  RESPONSE OF RODENTS TO HABITAT FRAGMENTATION IN COASTAL SOUTHERN CALIFORNIA , 1997 .

[80]  P. Becker,et al.  More about euglossine bees in Amazonian forest fragments , 1991 .

[81]  G. Powell,et al.  Population dynamics of male euglossine bees in Amazonian forest fragments , 1987 .

[82]  T. Tscharntke,et al.  Bioindication using trap‐nesting bees and wasps and their natural enemies: community structure and interactions , 1998 .

[83]  J. E. Bowers,et al.  Flowering phenology of six woody plants in the northern Sonoran Desert , 1994 .

[84]  C. Zachariades,et al.  Effects of Habitat Fragmentation on Pollinator Diversity and Plant Reproductive Success in Renosterveld Shrublands of South Africa , 2002 .

[85]  P. Kevan BLUEBERRY CROPS IN NOVA SCOTIA AND NEW BRUNSWICK—PESTICIDES AND CROP REDUCTIONS , 1977 .

[86]  Robert K. Colwell,et al.  Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness , 2001 .

[87]  Felipe Vivallo,et al.  Conservation Genetics of Potentially Endangered Mutualisms: Reduced Levels of Genetic Variation in Specialist versus Generalist Bees , 2005 .

[88]  Jaboury Ghazoul,et al.  Reproductive ecology of tropical forest trees in logged and fragmented habitats in Thailand and Costa Rica , 2001 .

[89]  N. Williams,et al.  Variation in Native Bee Faunas and its Implications for Detecting Community Changes , 2001 .

[90]  M. Archer The wasps and bees (Hymenoptera : Aculeata) of allerthorpe common before and after coniferization , 1989 .

[91]  R. Gillespie,et al.  Effects of Natural Forest Fragmentation on a Hawaiian Spider Community , 2004 .

[92]  Jane Memmott,et al.  Tolerance of pollination networks to species extinctions , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[93]  M. Aizen,et al.  HABITAT FRAGMENTATION, NATIVE INSECT POLLINATORS, AND FERAL HONEY BEES IN ARGENTINE, "CHACO SERRANO"' , 1994 .