Abstract
Seed predation may influence community assembly and invasion dynamics when seed predators preferentially select some seed species over others. However, the role of different seed predators and their preferences for seeds in multiple ecological contexts, including the endangered California sage scrub ecosystem, remain unresolved making predictions about which processes limit or promote invasions difficult. In addition, selection criteria, specifically how seed size and biogeographic origin (native versus invasive) influences selection, requires further research across multiple granivore guilds. We examined seed predator preference for common native and invasive seeds across small and large seed classes using seed dish experiments with motion-sensor video observation. We also quantified the relative importance of ants, birds, and mammals as seed predators in sage scrub. Community-wide, granivores preferred the small-seeded invasive mustard Brassica nigra, avoided the large-seeded invasive grass Bromus rubens and the native large-seeded shrub Encelia californica, and did not show significant selection or avoidance for the small-seeded native shrub Salvia apiana. Birds, notably California towhees (Melozone crissalis), were the most frequent granivore while rodents and ants rarely removed seeds. This study reveals that birds are important seed predators in California sage scrub and have the potential to contribute to biotic resistance to mustard invasions (Brassica nigra and potentially others).
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Data availability
The dataset is available in the Knowledge Network for Biocomplexity repository: https://knb.ecoinformatics.org/view/doi:10.5063/R78CMB.
Code availability
Code used in this study is available on Github at https://github.com/jloesberg/CSS_SeedPredator.
References
Aput LM, Farji-Brener AG, Pirk GI (2019) Effects of introduced plants on diet and seed preferences of Pogonomyrmex carbonarius (Hymenoptera: Formicidae) in the Patagonian Steppe. Environ Entomol 48:567–572. https://doi.org/10.1093/ee/nvz022
Bell DT, Muller CH (1973) Dominance of California annual grasslands by Brassica nigra. Am Midl Nat 90:277–299
Bricker M, Pearson D, Maron J (2010) Small-mammal seed predation limits the recruitment and abundance of two perennial grassland forbs. Ecology 91:85–92. https://doi.org/10.1890/08-1773.1
Briggs CM, Redak RA (2016) Seed selection by the Harvester Ant Pogonomyrmex rugosus (Hymenoptera: Formicidae) in coastal sage scrub: interactions with invasive plant species. Environ Entomol 45:983–990. https://doi.org/10.1093/ee/nvw042
Brown JH, Heske EJ (1990) Control of a desert-grassland transition by a keystone rodent guild. Science 250:1705–1707
Burger JC, Redak RA, Allen EB, Rotenberry JT, Allen MF (2003) Restoring arthropod communities in coastal sage scrub. Conserv Biol 17:460–467. https://doi.org/10.1046/j.1523-1739.2003.01325.x
Caspi T, Hartz LA, Soto Villa AE, Loesberg JA, Robins CR, Meyer WM III (2019) Impacts of invasive annuals on soil carbon and nitrogen storage in southern California depend on the identity of the invader. Ecol Evol 9:4980–4993. https://doi.org/10.1002/ece3.5104
Connolly BM, Pearson DE, Mack RN (2014) Granivory of invasive, naturalized, and native plants in communities differentially susceptible to invasion. Ecology 95:1759–1769. https://doi.org/10.1890/13-1774.1
Cox RD, Preston KL, Johnson RF, Minnich RA, Allen EB (2014) Influence of landscape-scale variables on vegetation conversion to exotic annual grassland in southern California, USA. Glob Ecol Conserv 2:190–203. https://doi.org/10.1016/j.gecco.2014.09.008
Crawley MJ (2000) Seed predators and plant population dynamics. In: Fenner M (ed) Seeds, the ecology of regeneration in plant communities, 2nd edn. CAB International, New York, pp 167–182
Crist TO, MacMahon JA (1992) Harvester ant foraging and shrub-steppe seeds: interactions of seed resources and seed use. Ecology 73:1768–1779
Crooks KR, Soulé ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566. https://doi.org/10.1038/23028
Cueto VR, Marone L, Lopez De Casenave J (2006) Seed preferences in sparrow species of the Monte desert, Argentina: implications for seed-granivore interactions. Auk 123:358–367. https://doi.org/10.1642/0004-8038(2006)123[358:SPISSO]2.0.CO;2
Davidson DW, Inouye RS, Brown JH (1984) Granivory in a desert ecosystem: experimental evidence for indirect facilitation of ants by rodents. Ecology 65:1780–1786. https://doi.org/10.2307/1937774
Davis FW, Stine PA, Stoms DM (1994) Distribution and conservation status of coastal sage scrub in southwestern California. J Veg Sci 5:743–756. https://doi.org/10.2307/3235887
Dellafiore CM, Fernández JBG, Vallés SM (2010) The rabbit (Oryctolagus cuniculus) as a seed disperser in a coastal dune system. Plant Ecol 206:251–261. https://doi.org/10.1007/s11258-009-9639-7
Dial KP (1988) Three sympatric species of Neotoma: dietary specialization and coexistence. Oecologia 76:531–537. https://doi.org/10.1007/BF00397865
Dylewski Ł, Ortega YK, Bogdziewicz M, Pearson DE (2020) Seed size predicts global effects of small mammal seed predation on plant recruitment. Ecol Lett 23:1024–1033. https://doi.org/10.1111/ele.13499
Elton C (1958) The ecology of invasions by animals and plants. University of Chicago Press, Chicago
Goldingay RL, Kelly PA, Williams DF (1997) The Kangaroo Rats of California: endemism and conservation of keystone species. Pacific Conserv Biol 3:47–60. https://doi.org/10.1071/PC970047
Heleno RH, Ross G, Everard A, Memmott J, Ramos JA (2011) The role of avian “seed predators” as seed dispersers. Ibis 153:199–203. https://doi.org/10.1111/j.1474-919X.2010.01088.x
Hulme PE (1998) Post-dispersal seed predation: consequences for plant demography and evolution. Perspect Plant Ecol Evol Syst 1:32–46. https://doi.org/10.1078/1433-8319-00050
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. https://doi.org/10.1016/S0169-5347(02)02499-0
Keeley JE (2001) Fire and invasive species in Mediterranean-climate ecosystems of California. Fire Conf 2000 First Natl Congr Fire Ecol Prev Manag Miscellane 11:81–94
Kelrick MI, MacMahon JA, Parmenter RR, Sisson DV (1986) Native seed preferences of shrub-steppe rodents, birds and ants: the relationships of seed attributes and seed use. Oecologia 68:327–337
Krebs C (1999) Ecological methodology, 2nd edn. Addison-Welsey Educational Publishers, Mento Park
Larios L, Pearson DE, Maron JL (2017) Incorporating the effects of generalist seed predators into plant community theory. Funct Ecol 31:1856–1867. https://doi.org/10.1111/1365-2435.12905
Linsdale JM (1946) The California ground squirrel: a record of observations made on the Hastings natural history reservation. University of California Press, Berkeley
Lucero JE (2018) Do seeds from invasive bromes experience less granivory than seeds from native congeners in the Great Basin Desert? Plant Ecol 219:1053–1061. https://doi.org/10.1007/s11258-018-0858-7
Lucero JE, Callaway RM (2018) Native granivores reduce the establishment of native grasses but not invasive Bromus tectorum. Biol Invasions 20:3491–3497. https://doi.org/10.1007/s10530-018-1789-x
Lucero JE, Schaffner U, Asadi G, Bagheri A, Rajabov T, Callaway RM (2019) Enemy release from the effects of generalist granivores can facilitate Bromus tectorum invasion in the Great Basin Desert. Ecol Evol 9:8490–8499. https://doi.org/10.1002/ece3.5314
MacMahon JA, Mull JF, Crist TO (2000) Harvester ants (Pogonomyrmex spp.): their community and ecosystem influences. Annu Rev Ecol Syst 31:265–291
Mares MA, Rosenzweig ML (1978) Granivory in North and South American deserts: rodents, birds, and ants. Ecology 59:235–241
Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc B Biol Sci 273:2575–2584. https://doi.org/10.1098/rspb.2006.3587
Maron JL, Pearson DE, Potter T, Ortega YK (2012) Seed size and provenance mediate the joint effects of disturbance and seed predation on community assembly. J Ecol 100:1492–1500. https://doi.org/10.1111/j.1365-2745.2012.02027.x
Meserve PL (1976) Habitat and resource utilization by rodents of a California coastal sage scrub community. J Anim Ecol 45:647–666
Parker T (2015) Seed bank divergence between Arctostaphylos Adans. (Ericaceae) and Ceanothus L. (Rhamnaceae) suggests different seed predator interactions. Ecol Mediterr 41:5–13
Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461. https://doi.org/10.1126/science.1121407
Pearson DE, Callaway RM, Maron JL (2011) Biotic resistance via granivory: establishment by invasive, naturalized, and native asters reflects generalist preference. Ecology 92:1748–1757. https://doi.org/10.1890/11-0164.1
Pearson DE, Potter T, Maron JL (2012) Biotic resistance: exclusion of native rodent consumers releases populations of a weak invader. J Ecol 100:1383–1390. https://doi.org/10.1111/j.1365-2745.2012.02025.x
Pearson DE, Hierro JL, Chiuffo M, Villarreal D (2014a) Rodent seed predation as a biotic filter influencing exotic plant abundance and distribution. Biol Invasions 16:1185–1196. https://doi.org/10.1007/s10530-013-0573-1
Pearson DE, Icasatti NS, Hierro JL, Bird BJ (2014b) Are local filters blind to provenance? Ant seed predation suppresses exotic plants more than natives. PLoS ONE 9:1–11. https://doi.org/10.1371/journal.pone.0103824
Petry WK, Kandlikar GS, Kraft NJB, Godoy O, Levine JM (2018) A competition–defence trade-off both promotes and weakens coexistence in an annual plant community. J Ecol 106:1806–1818. https://doi.org/10.1111/1365-2745.13028
Pirk GI, Lopez de Casenave J (2017) Ant interactions with native and exotic seeds in the Patagonian steppe: influence of seed traits, disturbance levels and ant assemblage. Plant Ecol 218:1255–1268. https://doi.org/10.1007/s11258-017-0764-4
Price M, Goldingay RL, Szychowski S, Waser N (1994) Managing Habitat for the Endangered Stephens’ Kangaroo Rat (Dipodomys stephensi): effects of Shrub Removal. Am Midl Nat 131:9–16
Purcell KL, Verner J (1998) Density and reproductive success of California towhees. Conserv Biol 12:442–450. https://doi.org/10.1111/j.1523-1739.1998.96354.x
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Riordan EC, Rundel PW (2014) Land use compounds habitat losses under projected climate change in a threatened California ecosystem. PLoS ONE 9:e86487. https://doi.org/10.1371/journal.pone.0086487
Rundel P (2007) Sage scrub. In: Barbour MG, Keeler-Wolf T, Schoenner AA (eds) Terrestrial vegetation of California. University of California Press, Berkeley, pp 208–228
Staubus WJ, Boyd ES, Adams TA, Spear DM, Dipman MM, Meyer WM III (2015) Ant communities in native sage scrub, non-native grassland, and suburban habitats in Los Angeles County, USA: conservation implications. J Insect Conserv 19:669–680. https://doi.org/10.1007/s10841-015-9790-5
Thompson DB, Brown JH, Spencer WD (1991) Indirect facilitation of granivorous birds by desert rodents: experimental evidence from foraging patterns. Ecology 72:852–863. https://doi.org/10.2307/1940587
Thomson DM, Meyer WM III, Whitcomb IF (In Review) Non-native plant removal and high rainfall years promote post-fire recovery of Artemisia californica in southern California sage scrub. PLoS ONE.
Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225–238
Vander Wall S, Kuhn K, Beck M (2005) Seed removal, seed predation, and secondary dispersal. Ecology 86:801–806
Warzecha B, Parker TV (2014) Differential post-dispersal seed predation drives chaparral seed bank dynamics. Plant Ecol 215:1313–1322. https://doi.org/10.1007/s11258-014-0389-9
Zona S (2017) Fruit and seed dispersal of Salvia L. (Lamiaceae): a review of the evidence. Bot Rev 83:195–212. https://doi.org/10.1007/s12229-017-9189-y
Acknowledgements
We acknowledge that this study took place on the traditional, ancestral, and unceded territory of the Gabrielino/Tongva peoples. Thank you to D. Thomson, the Williams Lab at UBC, and three anonymous reviewers for useful comments on the manuscript; N. Karnovksy for assistance with rodent identification; F. Jammes for help determining methods for making seeds infertile; C. Chase, C. Halligan, K. Madunich, and L. Thomey for field and lab assistance.
Funding
This study was funded by the Schenk Family Fund, the Bernard Field Station, and the Keck Science Department of the Claremont Colleges.
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JAL and WMM designed and performed the experiments; JAL analyzed the data and wrote the manuscript; WMM provided analysis advice and contributed to manuscript revisions.
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Loesberg, J.A., Meyer, W.M. Granivory in California sage scrub: implications for common plant invaders and ecosystem conservation. Plant Ecol 222, 1089–1100 (2021). https://doi.org/10.1007/s11258-021-01163-z
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DOI: https://doi.org/10.1007/s11258-021-01163-z