Small mammals limit tree population growth in an African savanna

Transcription

1 Maclean et al. 1 1 Running Head: Small mammals limit tree population growth 2 3 Small mammals limit tree population growth in an African savanna 4 5 Janet E. Maclean 1,2,3, Jacob R. Goheen 2,3, Todd M. Palmer 3,4, and Truman P. Young 3,5 6 1) Correspondence: maclean@zoology.ubc.ca 7 8 2) Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, BC V6T 1Z4, Canada. 9 3) Mpala Research Centre, Nanyuki, PO Box 555, Kenya. 10 4) Department of Zoology, University of Florida, Gainesville, FL 32611, USA. 11 5) Department of Plant Sciences, University of California, Davis, CA 95616, USA.

2 Maclean et al Abstract Tree abundance drives the structure and function of savanna ecosystems, underlying nutrient cycling, fire return intervals, soil-water relations, and patterns of biodiversity. In African savannas, large herbivores such as elephants, giraffes, and antelopes are widely regarded as primary biotic drivers of tree population dynamics, and are attributed key roles in maintaining the tree-grass codominance that typifies these systems. However, the potential role of more cryptic herbivores in regulating savanna structure and function has largely been ignored. Combining a long-term ungulate exclusion experiment, a six-year manipulation of small mammal densities, and retrospective demographic analyses, we show that small mammals suppress tree recruitment and strongly limit the population growth of trees. Further, we show that small mammals have greater impacts following the simulated extinction of ungulates and that the impacts of small mammal are comparable to those of ungulates in reducing tree population growth. We suggest that these cryptic consumers must be carefully considered as biologists work to understand how ecosystems will reorganize in the face of ongoing, global declines in ungulate populations Key words: herbivory, life table response experiment (LTRE), matrix model, rodent, savanna, seed predation, small mammal, tree recruitment, ungulate Introduction Savannas are a widespread and important biome, covering over 20% of the terrestrial earth s surface and accounting for the majority of the world s rangelands (Scholes and Archer 1997, Sankaran et al. 2005). Typified by co-dominating trees and grasses, savannas are home to the highest diversity and biomass of wild and domestic ungulates worldwide. While savanna

3 Maclean et al ecosystems have been intensively studied (Sinclair and Arcese 1995, du Toit et al. 2003, Sinclair et al. 2006), the processes that maintain the tree-grass co-dominance that typifies these systems remain contentious (van Langevelde et al. 2003, Sankaran et al. 2004). In African savannas in particular, the extent to which ungulates impose demographic bottlenecks by browsing and killing adult trees has triggered a multitude of studies, highlighting that ungulate effects can be contingent on precipitation (Sankaran et al. 2005, Holdo 2007), productivity (Pringle et al. 2007), fire (Dublin et al. 1990, van Langevelde et al. 2003), soil nutrients (Fornara and du Toit 2008), and other factors (Guldemond and Van Aarde 2008) While the growth and survival of adult trees is clearly important for tree population dynamics, a singular focus on this conspicuous life stage (and its conspicuous consumers) may obscure cryptic, but potentially critical, demographic processes underlying tree populations (Midgley and Bond 2001). Despite the profound impact of seed and seedling consumers on vegetation dynamics elsewhere (e.g., Brown and Heske 1990, Gomez 2005, Maron and Kauffman 2006, El-Bana 2009), the role of these consumers in structuring savanna vegetation has been almost completely ignored (but see Sharam et al. 2009). To fully understand the role of herbivory in regulating savanna ecosystems, the impact of cryptic consumers on tree demography must be considered alongside their more conspicuous counterparts The potential for seed and seedling consumers to suppress tree populations hinges both on the extent to which tree populations are limited by seed availability (Maron and Kauffman 2006), and on the relative importance of tree recruitment for population growth compared to adult growth and survival (Janzen 1970, Midgley and Bond 2001, Smith et al. 2003, Maron and Kauffman 2006). For long-lived species, rates of population growth typically are more sensitive to variation in adult growth and survival than to recruitment (Caswell 2001). However, the magnitude of seed

4 Maclean et al and seedling consumption may be sufficiently high to override variation in adult growth and survival, and in so doing drive population dynamics (Caswell 2001). Although small mammals are known to depress plant recruitment across terrestrial ecosystems (e.g., Maron and Crone 2006, MacDougall and Wilson 2007, Iob and Vieira 2008), it remains unclear whether their effects are strong enough to influence the overall long-term population growth of trees We compared the relative importance of wild ungulates, domestic ungulates (i.e., cattle), and small mammals (the dominant seed and seedling consumers at our sites; Keesing 2000, Goheen et al. 2004) in suppressing the population growth of Acacia drepanolobium, a monodominant tree abundant throughout much of East Africa (Pratt and Gwynne 1977, Angassa 2005). Using a series of large ungulate and small mammal exclosures, we determined tree population growth under eight experimentally-controlled herbivore communities over five years to answer the questions: 1) Through which demographic pathways are populations of A. drepanolobium limited?; 2) Do small mammals impact tree population growth?; and 3) Are impacts of small mammals on tree demography dependant on the presence of large ungulates? Methods 73 Data Collection We conducted our fieldwork between at Mpala Research Centre in the Laikipia District of central Kenya (0 17 N, E, 1800m ASL). The tree populations of our study occur within the Kenya Long-term Exclosure Experiment (KLEE), a replicated series of 4-ha plots through which combinations of wild ungulates and cattle are permitted access or selectively excluded using a series of herbivore barriers (Young et al. 1998). KLEE was established in 1995

5 Maclean et al and is underlain by black cotton soils, with A. drepanolobium comprising >95% of the overstory cover. For the purposes of our experiments, we targeted the following ungulate treatments in a complete 2 x 2 factorial design of cattle and wildlife treatments: 82 1) full fencing to exclude all large (> 15 kg) ungulates ) full fencing to exclude wild, large ungulates, but with cattle grazed six to eight times per year at intensities approximating the surrounding region (Young et al. 2005). 85 3) no fencing; wild ungulates have access but cattle are not allowed to graze. 86 4) no fencing; wild ungulates have access and cattle are grazed Wild ungulates that browse on A. drepanolobium that are excluded by KLEE fences include elephants (Loxodonta africana), giraffes (Giraffa camelopardalis), elands (Taurotragus oryx), and Grant s gazelles (Gazella granti). Non-excluded steinbuck (Raphicerus campestris) also browse A. drepanolobium. The dominant small mammal in this system is the northern pouched mouse (Saccostomus mearnsi), which comprises 85-90% of captures (Keesing 2000) In May and June 2004, we tagged 1389 A. drepanolobium trees and monitored their annual growth, reproduction, and survival over the subsequent five years. These focal trees were distributed approximately equally among the four herbivore treatments (range = 75 [lowest treatment] 202 [highest treatment]), across three replicate blocks. For each tree in each year, we noted whether individuals were reproductive, and measured height to the nearest 5 cm and length of the longest crown axis to the nearest 10 cm. Based on logistic generalized linear models and model selection procedures (Burnham and Anderson 2002), crown breadth was a better determinant of tree reproduction and survival than was height. Therefore, we used crown breadth as a classifying variable to group trees in the subsequent matrix analysis (Morris and Doak 2002).

6 Maclean et al We recorded the number of saplings recruiting in the presence and absence of small mammals for 24 reproductive trees in each plot in each year with the exception of 2007 (when all 1389 trees failed to reproduce) and in 2008 (when prolonged drought prevented germination). All seeds produced by these 24 trees were collected and counted, after which all seeds not damaged by bruchid beetles were sown in the field in close proximity to their parent tree. We believe that these methods did not differ significantly from natural dispersal, because all recently germinated saplings noted over the course of this study occurred within 3 m of parent trees (Goheen et al. in review). These seeds were divided equally between four treatments to investigate the role of seed consumption by insects, small mammals, and birds in reducing the number of surviving saplings produced per tree. These treatments were (i) exclusion of insects, small mammals and birds; (ii) exclusion of small mammals and birds; (iii) exclusion of birds only; and (iv) uncaged control (see Goheen et al. in review for methods and results of recruitment experiments). Germination did not differ significantly between treatments (i) and (ii) or treatments (iii) and (iv), so saplings surviving to the following year in each of these treatment pairs were pooled and multiplied by two to give sapling production for individual trees in the presence and absence of small mammals. See Goheen et al (in review) for further details on results of recruitment experiments. A. drepanolobium does not have a seed bank (Okello and Young 2000). 118 Life Table Response Experiment (LTRE) We constructed stage-structured projection matrices (sensu Caswell 2001) using the demographic data collected from the focal trees in each treatment combination each year, yielding a total of 40 matrices (4 ungulate treatments x 2 small mammal treatments x 5 transition years). We pooled data from trees across all three replicates of each treatment to construct a single summary matrix for each treatment-year combination (sensu Horvitz and Schemske 1995). This method reduces

7 Maclean et al poorly-parameterized transition probabilities (Horvitz and Schemske 1995, Morris and Doak 2002, Bruna and Oli 2005), and therefore it is preferable to calculating average transitions as the mean of the transitions over the three replicates. We interpreted the dominant eigenvalue of each matrix as the asymptotic geometric growth rate (λ) of the population under that treatment combination (Caswell 2001, Morris and Doak 2002). Lambda represents a comprehensive measure of demographic success and therefore can be used to compare the average fitness of individuals under different experimental conditions (Horvitz and Schemske 1995). We compared λ under each treatment in a life table response experiment (LTRE) framework. All analyses were carried out using R version (R Development Core Team 2008) and the add-on package demogr version (Jones 2007) LTREs are a form of retrospective matrix analysis permitting scientists to test for responses of λ to different experimental treatments (Caswell 2001). LTREs utilize observed differences in demographic transition rates resulting from experimental manipulations to reveal overall differences in population growth between the treatments of interest. Critically, LTREs allow data from applied, short-term experimental manipulations to reveal expected differences in long-term demographic trends for populations in each treatment. The λ of populations under each treatment is compared, and then decomposed into the contributions of each transition or fertility element to the difference in population growth rate between treatments (Δλ). Contributions are assessed by multiplying the sensitivities of matrix elements (calculated midway between the two treatment matrices) by the difference between associated elements for each of the two matrices in the LTRE, thereby revealing the demographic transitions underlying Δλ (see Appendix 1 for a full discussion of LTRE procedures).

8 Maclean et al For each year, we compared λ for each of the eight treatments. We considered λ as differing significantly among treatments if 95% confidence intervals did not overlap (Bruna and Oli 2005). This method of assessing statistical significance is appropriate because statistics resulting from matrix calculations are non-linear functions of data with unknown distributions, so traditional significance tests cannot be applied (Caswell 2001). Confidence intervals were estimated by taking values of λ from the 2.5 and 97.5 quantiles of a distribution generated from 2000 bootstrap re-samples of the 40 treatment-year summary matrices. In each bootstrap sample, the focal trees for that treatment-year combination were resampled with replacement and all the matrix elements were re-estimated to reconstruct a new, bootstrapped matrix for every iteration. Thus, resampling occurred at the level of individual trees rather than matrix elements, so as to maintain any covariance structure among the elements (Caswell 2001) Matrices were compared between all sets of plots where only one experimental factor differed (e.g., the presence or absence of small mammals, wild ungulates, or cattle, for a total of 12 comparisons per year). For each of these comparisons, the contributions of all fertility matrix entries (row 1) and of all stasis, growth and regression transition entries (rows 2-5) were summed to give their overall contribution to Δλ (Bruna and Oli 2005). This reveals whether small mammals and large ungulates affected population growth of trees through recruitment or through adult growth and survival We calculated annual rainfall between our survey periods from monthly rain gauge measures. We then conducted linear regression between λ and annual rainfall in the presence and absence of large ungulates and small mammals to ascertain if interannual variation in λ was related to differences in rainfall.

9 Maclean et al Results Small mammals reduced the population growth of trees, especially in treatments excluding wild ungulates during 2004 and 2005 (Fig. 1). When tree seeds and seedlings were accessible to small mammals, values of λ were consistently below 1, whereas in the absence of small mammals values of λ often exceeded 1, significantly so in 2004 and 2005 (λ > 1 indicates population growth; λ < 1 indicates population decline). Across years, wild ungulates consistently decreased λ, again causing a significant decrease in λ in 2004 and 2005 (Fig. 1). Cattle exerted a small positive influence on λ, although this effect was not statistically significant for any year (Fig. 1) Small mammal impacts on λ were mediated entirely through tree fertilities, whereas wild ungulate impacts were mediated predominantly through adult growth and survival, and occasionally also through tree fertilities (Fig. 2). Small mammals had no effect on λ in 2007 (when trees failed to reproduce) or 2008 (when drought prevented germination of seeds). Wild ungulates similarly had no effect on λ in 2008 (Fig. 2) We detected no significant effect of rainfall on λ in control plots (R 2 =0.28, d.f.=3, P=0.36) or exclusion plots (R 2 =0.02, d.f.=3, P=0.84) Discussion Our results show that small mammals can strongly suppress tree population growth, and that the magnitude of this suppression can equal that of wild ungulates. The effect of small mammals on savanna trees was variable, having the largest influence when wild ungulates were

10 Maclean et al excluded, and in years when trees had high seed production (seed production of A. drepanolobium was significantly greater in the absence of wild ungulates, and was highest in 2005 (Goheen et al. 2007)). Therefore, small mammals effectively buffered against tree population growth, having maximal impacts when other factors (e.g., wild ungulates, seed limitation) were minimized. Our study highlights the potentially critical role of this cryptic guild of consumers in driving the demographic rates of tree populations Wild ungulates are widely recognized to reduce the growth, reproduction, and survival of adult trees (Dublin et al. 1990, Midgley and Bond 2001, Deveny and Fox 2006), concordant with our results showing that wild ungulates consistently decreased λ. We revealed that cattle exerted a small positive influence on λ, although this effect was not statistically significant for any year. This finding also concurs with previous work in this system demonstrating that cattle grazing facilitates both sapling recruitment and growth of adult trees by reducing competition from grasses (Riginos and Young 2007, Riginos 2009). Prior studies have shown that both wild and domestic ungulates can also indirectly facilitate tree recruitment by suppressing abundances of small mammals, thereby exerting an indirect, positive effect on tree populations (Goheen et al. 2007, Goheen et al. in review). This indirect positive effect is illustrated by our finding that recruitment limitation of trees by small mammals is stronger where ungulates have been excluded. However, across all years, the net effect of wild ungulates was negative: the direct, negative effect of wild ungulates on tree growth and survival overrode indirect facilitation of tree recruitment. This negative net effect was due largely to the high sensitivity of λ to the survival of large trees (see Caswell 2001), whereby slight reductions in the transition rates for adult growth and stasis effectively reduced population growth.

11 Maclean et al Lambda was variable across the five years of our study, likely due to inter-annual fluctuations in resources (see also Scholes and Archer 1997, Sankaran et al. 2005). Inter-annual variability in λ was reduced where small mammals had access to tree seeds and seedlings. This reflects the ability of herbivores of very different sizes to impose demographic restrictions on populations of savanna trees. Our results therefore support the hypothesis that herbivores can suppress tree population growth below the potential levels bounded by resource limitation (Sankaran et al. 2005), and suggest that tree encroachment likely would occur in the absence of both small mammals and wild ungulates In savanna ecosystems, population growth of trees often is envisaged as episodic, with positive population growth occurring during narrow windows of high rainfall (du Toit et al. 2003, Sankaran et al. 2005). Annual rainfall during our study ranged from 732mm ( ) to 465mm ( ). These years represent the second highest and second lowest annual rainfall recorded over the 11-year time series at Mpala; thus, we have included years representative of the majority of annual rainfall events. However, we detected no significant effect of rainfall on λ in plots to which all herbivores had access nor in plots from which all herbivores were excluded, implying our results and conclusions are robust to variability in rainfall While fire can influence tree population dynamics (Scholes and Archer 1997, Higgins et al. 2000, Sankaran et al. 2005), it has been suppressed since the early 1960s in Laikipia. In addition, A. drepanolobium is a classic fire tolerant species, with saplings re-sprouting readily following controlled burns (Okello et al. 2008). Thus, the results of our study should be consistent with patterns of population growth in areas exposed to fires, even though fire now is largely absent in Laikipia.

12 Maclean et al To our knowledge, ours is the first cradle to grave study of tree population dynamics to simultaneously investigate the role of both large and small herbivores in driving tree demography. While the capacity of small mammals to reduce survival of tree seeds and seedlings has been documented across a range of systems (Weltzin et al. 1997, Schnurr et al. 2004, de Mattia et al. 2006, Longland 2007), our results provide an important advance by demonstrating that small mammals can limit overall tree population growth by serving as demographic filters to recruitment. Counterintuitively, we show that small mammals are comparable to large ungulates in limiting tree population growth, and that the magnitude of these effects depends on the presence of ungulates themselves In African savannas, landscape change often is manifested by altered browsing regimes stemming from the extirpation or overabundance of large mammals, particularly elephants (Dublin et al. 1990, Augustine and McNaughton 2004). Our study suggests that seed and seedling consumers may buffer against tree encroachment following local extinctions of ungulates in savanna systems. Effective rangeland management relies on an understanding of how species interactions influence range quality. We have established the potential role that small mammals play in mitigating tree encroachment in African savannas. We hope that our study will lead to an enhanced appreciation of the multiple diverse pathways through which tree populations are regulated in savanna ecosystems. 251 Acknowledgements We thank Abdikadir Ali Hassan and Simon Lima for field assistance. We also thank the Mpala Research Centre and its staff for their logistical support. JEM acknowledges the University of British Columbia for funding. JRG acknowledges the Natural Sciences and Engineering Research Council (NSERC) of Canada, the American Society of Mammalogists, the Smithsonian Tropical

13 Maclean et al Research Institute, and the U.S. Environmental Protection Agency for funding. TMP acknowledges the U.S. National Science Foundation (DEB , DEB ) for funding. The exclosure plots were built and maintained by grants from the James Smithson Fund of the Smithsonian Institution (to A.P. Smith), The National Geographic Society ( ), The National Science Foundation (LTREB BSR , , and ) and the African Elephant Program of the U.S. Fish and Wildlife Service ( G563) (to T.P. Young).

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18 Maclean et al Figure Legends Fig. 1: Projected rates of population growth (λ) for each wild ungulate, cattle, and small mammal treatment. Rates of population growth in plots accessible to small mammals (grey bars) never significantly exceeded replacement (λ 1), whereas λ from small mammal exclusion plots (white bars) often was greater than 1, showing a higher rate of population growth. The dashed line shows λ = 1 (no positive nor negative population growth). Data are presented as projected λ ± bootstrapped 95% confidence intervals. The final panel shows the mean value of projected lambda over all five years ± 95% confidence intervals calculated from 2000 bootstrap resamples of the entire analysis (resampling occurs at the individual tree level), with a new mean value of lambda calculated in each iteration. We considered non-overlapping confidence intervals to indicate statistically significant differences in λ Fig. 2: Contributions to the increase in projected population growth (Δλ) caused by the exclusion of small mammals or wild ungulates. The overall difference in lambda is divided into the summed contributions from the fertilities (grey bars) or the growth, regression and survival transitions (white bars). The total height of the bars shows the overall increase in λ caused by excluding small mammals (left column) or wild ungulates (right column). Contributions are displayed for each of the four possible treatment combinations each year. Small mammals had no effect on population growth in 2007 or 2008, and wild ungulates had no effect in 2008.

19 Maclean et al Fig. 1

20 Maclean et al Fig. 2