Skip to main content
Top
Published in: Urban Ecosystems 6/2017

20-04-2017

Soil lead contamination decreases bee visit duration at sunflowers

Authors: Frances S. Sivakoff, Mary M. Gardiner

Published in: Urban Ecosystems | Issue 6/2017

Log in

Activate our intelligent search to find suitable subject content or patents.

search-config
loading …

Abstract

Legacies of lead contamination present challenges in the management of urban greenspaces for beneficial insect conservation. In particular, the sublethal effects of lead contamination on bee foraging behavior could negatively impact plant-pollinator interactions and the sustainability of urban agriculture. It is difficult, however, to distinguish between differences in foraging behavior caused by lead contamination directly as compared to differences resulting from variation in floral traits, which can also be affected by contamination. We compared the foraging behavior of bees, specifically the number of visits and visit duration, at sunflowers grown in lead-contaminated and uncontaminated soils. We also measured soil lead contamination’s effects on sunflower morphological traits. While the number of visits a sunflower head received was not affected by soil lead contamination, bee visit duration was shorter at sunflowers grown in lead contaminated soil. This effect of lead contamination on visit duration was not mediated by sunflower floral traits, which were themselves affected by lead contamination. The inability of bees to distinguish between sunflowers grown in contaminated vs. uncontaminated soil prior to visitation suggests a possible bioaccumulation pathway for lead in bees.

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

  • über 102.000 Bücher
  • über 537 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Finance + Banking
  • Management + Führung
  • Marketing + Vertrieb
  • Maschinenbau + Werkstoffe
  • Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

  • über 67.000 Bücher
  • über 390 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Maschinenbau + Werkstoffe




 

Jetzt Wissensvorsprung sichern!

Appendix
Available only for authorised users
Literature
go back to reference Adesodun JK, Atayese MO, Agbaje TA, Osadiaye BA, Mafe OF, Soretire AA (2010) Phytoremediation potentials of sunflowers (Tithonia diversifolia and Helianthus annuus) for metals in soils contaminated with zinc and lead nitrates. Water Air Soil Pollut 207:195–201CrossRef Adesodun JK, Atayese MO, Agbaje TA, Osadiaye BA, Mafe OF, Soretire AA (2010) Phytoremediation potentials of sunflowers (Tithonia diversifolia and Helianthus annuus) for metals in soils contaminated with zinc and lead nitrates. Water Air Soil Pollut 207:195–201CrossRef
go back to reference Al Naggar YA, Naiem E-SA, Seif AI, Mona MH (2013) Honey bees and their products as a bio-indicator of environmental pollution with heavy metals. Mellifera 13:10–20 Al Naggar YA, Naiem E-SA, Seif AI, Mona MH (2013) Honey bees and their products as a bio-indicator of environmental pollution with heavy metals. Mellifera 13:10–20
go back to reference Antonovics J, Bradshaw AD, Turner R (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85CrossRef Antonovics J, Bradshaw AD, Turner R (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85CrossRef
go back to reference Bargańska Ż, Ślebioda M, Namieśnik J (2016) Honey bees and their products: Bioindicators of environmental contamination. Crit Rev Environ Sci Technol 46:235–248CrossRef Bargańska Ż, Ślebioda M, Namieśnik J (2016) Honey bees and their products: Bioindicators of environmental contamination. Crit Rev Environ Sci Technol 46:235–248CrossRef
go back to reference Boonyapookana B, Parkplan P, Techapinyawat S, DeLaune RD, Jugsujinda A (2005) Phytoaccumulation of lead by sunflower (Helianthus annuus), tobacco (Nicotiana tabacum), and vetiver (Vetiveria zizanioides). J Environ Sci Health A 40:117–137CrossRef Boonyapookana B, Parkplan P, Techapinyawat S, DeLaune RD, Jugsujinda A (2005) Phytoaccumulation of lead by sunflower (Helianthus annuus), tobacco (Nicotiana tabacum), and vetiver (Vetiveria zizanioides). J Environ Sci Health A 40:117–137CrossRef
go back to reference Bromenshenk JJ, Carlson S, Simpson J, Thomas J (1985) Pollution monitoring of Puget sound with honey bees. Science 227:632–634CrossRefPubMed Bromenshenk JJ, Carlson S, Simpson J, Thomas J (1985) Pollution monitoring of Puget sound with honey bees. Science 227:632–634CrossRefPubMed
go back to reference Brown SL, Chaney RL, Hettiarachchi GM (2016) Lead in urban soils: a real or perceived concern for urban agriculture? J Environ Qual 45:26–36CrossRefPubMed Brown SL, Chaney RL, Hettiarachchi GM (2016) Lead in urban soils: a real or perceived concern for urban agriculture? J Environ Qual 45:26–36CrossRefPubMed
go back to reference Citak D, Silici S, Tuzen M, Soylak M (2012) Determination of toxic and essential elements in sunflower honey from Thrace region, Turkey. Int J Food Sci Technol 47:107–113CrossRef Citak D, Silici S, Tuzen M, Soylak M (2012) Determination of toxic and essential elements in sunflower honey from Thrace region, Turkey. Int J Food Sci Technol 47:107–113CrossRef
go back to reference Cutright T, Gunda N, Kurt F (2010) Simultaneous hyperaccumulation of multiple heavy metals by Helianthus annuus grown in a contaminated sandy-loam soil. Int J Phytorem 12:562–573CrossRef Cutright T, Gunda N, Kurt F (2010) Simultaneous hyperaccumulation of multiple heavy metals by Helianthus annuus grown in a contaminated sandy-loam soil. Int J Phytorem 12:562–573CrossRef
go back to reference Devillers J, Pham-Delègue M-H (2002) Honey bees: estimating the environmental impact of chemicals. Taylor and Francis, LondonCrossRef Devillers J, Pham-Delègue M-H (2002) Honey bees: estimating the environmental impact of chemicals. Taylor and Francis, LondonCrossRef
go back to reference Di N, Hladun KR, Zhang K, Liu T-X, Trumble JT (2016) Laboratory bioassays on the impact of cadmium, copper and lead on the development and survival of honeybee (Apis mellifera L.) larvae and foragers. Chemosphere 152:530–538CrossRefPubMed Di N, Hladun KR, Zhang K, Liu T-X, Trumble JT (2016) Laboratory bioassays on the impact of cadmium, copper and lead on the development and survival of honeybee (Apis mellifera L.) larvae and foragers. Chemosphere 152:530–538CrossRefPubMed
go back to reference Fox J, Weisberg S (2011) An {R} companion to applied regression, Second edn. Sage, Thousand Oaks Fox J, Weisberg S (2011) An {R} companion to applied regression, Second edn. Sage, Thousand Oaks
go back to reference Free JB, Williams IH, Pinsent R, Townshend A, Basi MS, Graham CL (1983) Using foraging honeybees to sample an area for trace-metals. Environ Int 9:9–12CrossRef Free JB, Williams IH, Pinsent R, Townshend A, Basi MS, Graham CL (1983) Using foraging honeybees to sample an area for trace-metals. Environ Int 9:9–12CrossRef
go back to reference Gardiner MM, Burkman CE, Prajzner SP (2013) The value of urban vacant land to support arthropod biodiversity and ecosystem services. Environ Entomol 42:1123–1136CrossRefPubMed Gardiner MM, Burkman CE, Prajzner SP (2013) The value of urban vacant land to support arthropod biodiversity and ecosystem services. Environ Entomol 42:1123–1136CrossRefPubMed
go back to reference Gardiner MM, Prajzner SP, Burkman CE, Albro S, Grewal PS (2014) Vacant land conversion to community gardens: influences on generalist arthropod predators and biocontrol services in urban greenspaces. Urban Ecosyst 17:101–122CrossRef Gardiner MM, Prajzner SP, Burkman CE, Albro S, Grewal PS (2014) Vacant land conversion to community gardens: influences on generalist arthropod predators and biocontrol services in urban greenspaces. Urban Ecosyst 17:101–122CrossRef
go back to reference Hladun KR, Parker DR, Trumble JT (2011) Selenium accumulation in the floral tissues of two Brassicaceae species and its impact on floral traits and plant performance. Environ Exp Bot 74:90–97CrossRef Hladun KR, Parker DR, Trumble JT (2011) Selenium accumulation in the floral tissues of two Brassicaceae species and its impact on floral traits and plant performance. Environ Exp Bot 74:90–97CrossRef
go back to reference Hladun KR, Parker DR, Tran KD, Trumble JT (2013) Effects of selenium accumulation on phytotoxicity, herbivory, and pollination ecology in radish (Raphanus sativus L.) Environ Pollut 172:70–75CrossRefPubMed Hladun KR, Parker DR, Tran KD, Trumble JT (2013) Effects of selenium accumulation on phytotoxicity, herbivory, and pollination ecology in radish (Raphanus sativus L.) Environ Pollut 172:70–75CrossRefPubMed
go back to reference Hu LT, Bentler PM (1999) Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Model 6:1–55CrossRef Hu LT, Bentler PM (1999) Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Model 6:1–55CrossRef
go back to reference Jennings AA, Petersen EJ (2006) Variability of North American regulatory guidance for heavy metal contamination of residential soil. J Environ Eng Sci 5:485–508 Jennings AA, Petersen EJ (2006) Variability of North American regulatory guidance for heavy metal contamination of residential soil. J Environ Eng Sci 5:485–508
go back to reference Kastori R, Plesnicar M, Sakac Z, Pankovic D, Arsenijevic-Maksimovic I (1998) Effect of excess lead on sunflower growth and photosynthesis. J Plant Nutr 21:75–85CrossRef Kastori R, Plesnicar M, Sakac Z, Pankovic D, Arsenijevic-Maksimovic I (1998) Effect of excess lead on sunflower growth and photosynthesis. J Plant Nutr 21:75–85CrossRef
go back to reference Kevan PG (1999) Pollinators as bioindicators of the state of the environment: species, activity and diversity. Agric Ecosyst Environ 74:373–393CrossRef Kevan PG (1999) Pollinators as bioindicators of the state of the environment: species, activity and diversity. Agric Ecosyst Environ 74:373–393CrossRef
go back to reference Kohrman H, Chamberlain CP (2014) Heavy metals in produce from urban farms in the San Francisco Bay Area. Food Addit Contam, Part B 7:127–134CrossRef Kohrman H, Chamberlain CP (2014) Heavy metals in produce from urban farms in the San Francisco Bay Area. Food Addit Contam, Part B 7:127–134CrossRef
go back to reference Leita L, Muhlbachova G, Cesco S, Barbattini R, Mondini C (1996) Investigation of the use of honey bees and honey bee products to assess heavy metals contamination. Environ Monit Assess 43:1–9CrossRefPubMed Leita L, Muhlbachova G, Cesco S, Barbattini R, Mondini C (1996) Investigation of the use of honey bees and honey bee products to assess heavy metals contamination. Environ Monit Assess 43:1–9CrossRefPubMed
go back to reference Matteson KC, Ascher JS, Langellotto GA (2008) Bee richness and abundance in New York City urban gardens. Ann Entomol Soc Am 101:140–150 Matteson KC, Ascher JS, Langellotto GA (2008) Bee richness and abundance in New York City urban gardens. Ann Entomol Soc Am 101:140–150
go back to reference Meindl GA, Ashman T-L (2013) The effects of aluminum and nickel in nectar on the foraging behavior of bumblebees. Environ Pollut 177:78–81CrossRefPubMed Meindl GA, Ashman T-L (2013) The effects of aluminum and nickel in nectar on the foraging behavior of bumblebees. Environ Pollut 177:78–81CrossRefPubMed
go back to reference Meindl GA, Ashman T-L (2014) Nickel accumulation by Streptanthus polygaloides (Brassicaceae) reduces floral visitation rate. J Chem Ecol 40:128–135CrossRefPubMed Meindl GA, Ashman T-L (2014) Nickel accumulation by Streptanthus polygaloides (Brassicaceae) reduces floral visitation rate. J Chem Ecol 40:128–135CrossRefPubMed
go back to reference Meindl GA, Ashman T-L (2015) Effects of floral metal accumulation on floral visitor communities: introducing the elemental filter hypothesis. Am J Bot 102:379–389CrossRefPubMed Meindl GA, Ashman T-L (2015) Effects of floral metal accumulation on floral visitor communities: introducing the elemental filter hypothesis. Am J Bot 102:379–389CrossRefPubMed
go back to reference Mitchell RJ, Karron JD, Holmquist KG, Bell JM (2004) The influence of Mimulus ringens floral display size on pollinator visitation patterns. Funct Ecol 18:116–124CrossRef Mitchell RJ, Karron JD, Holmquist KG, Bell JM (2004) The influence of Mimulus ringens floral display size on pollinator visitation patterns. Funct Ecol 18:116–124CrossRef
go back to reference Mogren CL, Trumble JT (2010) The impacts of metals and metalloids on insect behavior. Entomol Exp Appl 135:1–17CrossRef Mogren CL, Trumble JT (2010) The impacts of metals and metalloids on insect behavior. Entomol Exp Appl 135:1–17CrossRef
go back to reference Mok H-F, Williamson VG, Grove JR, Burry K, Barker SF, Hamilton AJ (2014) Strawberry fields forever? Urban agriculture in developed countries: a review. Agron Sustain Dev 34:21–43CrossRef Mok H-F, Williamson VG, Grove JR, Burry K, Barker SF, Hamilton AJ (2014) Strawberry fields forever? Urban agriculture in developed countries: a review. Agron Sustain Dev 34:21–43CrossRef
go back to reference Parmentier L, Meeus I, Cheroutre L, Mommaerts V, Louwye S, Smagghe G (2014) Commercial bumblebee hives to assess an anthropogenic environment for pollinator support: a case study in the region of Ghent (Belgium). Environ Monit Assess 186:2357–2367CrossRefPubMed Parmentier L, Meeus I, Cheroutre L, Mommaerts V, Louwye S, Smagghe G (2014) Commercial bumblebee hives to assess an anthropogenic environment for pollinator support: a case study in the region of Ghent (Belgium). Environ Monit Assess 186:2357–2367CrossRefPubMed
go back to reference Perugini M, Manera M, Grotta L, Abete MC, Tarasco R, Amorena M (2011) Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves: honeybees as bioindicators. Biol Trace Elem Res 140:170–176 Perugini M, Manera M, Grotta L, Abete MC, Tarasco R, Amorena M (2011) Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves: honeybees as bioindicators. Biol Trace Elem Res 140:170–176
go back to reference Pisa LW et al (2015) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68–102 Pisa LW et al (2015) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68–102
go back to reference R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
go back to reference Rosseel Y (2012) Lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36CrossRef Rosseel Y (2012) Lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36CrossRef
go back to reference Ruschioni S, Riolo P, Minuz RL, Stefano M, Cannella M, Porrini C, Isidoro N (2013) Biomonitoring with honeybees of heavy metals and pesticides in nature reserves of the Marche region (Italy). Biol Trace Elem Res 154:226–233CrossRefPubMed Ruschioni S, Riolo P, Minuz RL, Stefano M, Cannella M, Porrini C, Isidoro N (2013) Biomonitoring with honeybees of heavy metals and pesticides in nature reserves of the Marche region (Italy). Biol Trace Elem Res 154:226–233CrossRefPubMed
go back to reference Satta A, Verdinelli M, Ruiu L, Buffa F, Salis S, Sassu A, Floris I (2012) Combination of beehive matrices analysis and ant biodiversity to study heavy metal pollution impact in a post-mining area (Sardinia, Italy). Environ Sci Pollut Res 19:3977–3988CrossRef Satta A, Verdinelli M, Ruiu L, Buffa F, Salis S, Sassu A, Floris I (2012) Combination of beehive matrices analysis and ant biodiversity to study heavy metal pollution impact in a post-mining area (Sardinia, Italy). Environ Sci Pollut Res 19:3977–3988CrossRef
go back to reference Schemske DW, Horvitz CC (1988) Plant animal interactions and fruit production in a neotropical herb: a path analysis. Ecology 69:1128–1137CrossRef Schemske DW, Horvitz CC (1988) Plant animal interactions and fruit production in a neotropical herb: a path analysis. Ecology 69:1128–1137CrossRef
go back to reference Schindelin J et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMed Schindelin J et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMed
go back to reference Singh A, Prasad SM (2011) Reduction of heavy metal load in food chain: technology assessment. Rev Environ Sci Biotechnol 10:199–214CrossRef Singh A, Prasad SM (2011) Reduction of heavy metal load in food chain: technology assessment. Rev Environ Sci Biotechnol 10:199–214CrossRef
go back to reference Stavert JR, Liñán-Cembrano G, Beggs JR, Howlett BG, Pattemore DE, Bartomeus I (2016) Hairiness: the missing link between pollinators and pollination. PeerJ 4:e2779CrossRefPubMedPubMedCentral Stavert JR, Liñán-Cembrano G, Beggs JR, Howlett BG, Pattemore DE, Bartomeus I (2016) Hairiness: the missing link between pollinators and pollination. PeerJ 4:e2779CrossRefPubMedPubMedCentral
go back to reference van der Steen JJM, de Kraker J, Grotenhuis T (2012) Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.) Environ Monit Assess 184:4119–4126CrossRefPubMed van der Steen JJM, de Kraker J, Grotenhuis T (2012) Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.) Environ Monit Assess 184:4119–4126CrossRefPubMed
go back to reference Venables WN, Ripley BD (2002) Modern applied statistics with S, Fourth edn. Springer, New YorkCrossRef Venables WN, Ripley BD (2002) Modern applied statistics with S, Fourth edn. Springer, New YorkCrossRef
Metadata
Title
Soil lead contamination decreases bee visit duration at sunflowers
Authors
Frances S. Sivakoff
Mary M. Gardiner
Publication date
20-04-2017
Publisher
Springer US
Published in
Urban Ecosystems / Issue 6/2017
Print ISSN: 1083-8155
Electronic ISSN: 1573-1642
DOI
https://doi.org/10.1007/s11252-017-0674-1

Other articles of this Issue 6/2017

Urban Ecosystems 6/2017 Go to the issue