Long-term population dynamics of small mammals in tropical dry forests, effects of unusual climate events, and implications for management and conservation☆
Introduction
The fate of any population, in very simple terms, depends on the factors affecting its survival and reproduction. Such factors can be broadly classified as intrinsic (i.e., density-dependent) or extrinsic (i.e., density-independent), based on their relationship or effects on population dynamics (Royama, 1992). Understanding the effects of intrinsic and extrinsic factors on population dynamics is particularly relevant in the face of the current massive human-induced environmental impacts (Brown, 2014)
In Royama’s framework, simple climate factors (temperature, rainfall and wind) are exogenous factors that may affect survival and reproduction directly, as there is a relationship between per capita rate of change and population density. The effect of exogenous variables on the per capita rate of population change can therefore be analyzed independently of population density. However, climate may also affect populations by influencing a limiting resource, such as food and water sources. In this case, its effect can be evaluated only in conjunction with population density (Royama, 1992). Thus, the relationship between climate and population density characterizes the per capita share of the resources and the competition strength for a given species (Berryman, 2003, Berryman and a, , 2001, Lima et al., 2008a, Lima et al., 2008b, Royama, , 1992, Valone et al., 1995).
Long-term population dynamics studies have spearheaded the development of this discipline (Elton and Nicholson, 1941, Elton, 1924, Lima et al., 2008a, Lima et al., 2008b). From these seminal works, we have been able understand that population dynamics of small mammals at higher-latitude temperate forests and grasslands are commonly related to predation and seasonality. Such populations show nonlinear dynamics with complex time lags. Extrinsic events in previous years can be major factors influencing dynamics (Ekerholm et al., 2001, Ergon et al., 2011, Hoset et al., 2009, Krebs and Boonstra, 1978, Lima, 2001, Lima et al., 2006a, Wang et al., 2001). However, aside from these well-known studies, most studies of population dynamics to date have been short-term, which can be misleading in understanding population patterns and processes (Berryman, 2003, Berryman, 1992, Berryman and a, , 2001, Berryman and Lima, 2006, Elton and Nicholson, 1941, Elton, 1924, Turchin and Taylor, 2007).
Recent studies of small-mammal dynamics have attempted to determine some of the factors affecting these dynamics. In northern mid-latitudes, in arid areas, some studies have found that small-mammal populations are affected by interspecific interactions and climatic factors, particularly atypical rainfall events, leading to local extinction and community-structure changes that can diminish taxonomic and functional diversity (Brown, 1973, Ernest et al., 2000, Fargione et al., 2003, Lima et al., 2008a, Lima et al., 2008b). In South American arid and semi-arid grasslands and shrublands, climate, especially El Niño–Southern Oscillation (ENSO), can strongly influence small-mammal population dynamics by causing sudden increases in resource availability (primary productivity), triggering effects such as spectacular population blooms of invasive species (Crespin and Lima, 2006, Jaksic and Lima, 2003, Letnic and Dickman, 2006, Lima, 2001, Lima et al., 1999, Lima and Jaksic, 1999). However, evaluations of long-term population dynamics are lacking, especially for tropical regions (Brown, 2014).
Human-induced global climate disruption is a major cause of biodiversity loss, and it is expected to worsen. Projections include temperature increase, changes in rainfall patterns, and higher probabilities of extreme climate events (Ernest et al., 2000, Lima et al., 2008a, Lima et al., 2008b, Thibault and Brown, 2008). For instance, strong hurricanes have increased by up to 20% in Australia (Hughes, 2003, Hughes, 2000, Williams et al., 2003). The most recent years have been climatically atypical for North America, with simultaneous high-category hurricanes in the Pacific Ocean. The strongest hurricane ever recorded in the eastern Pacific Ocean, Patricia, made landfall exactly where this study was performed in October 2015 (NOAA, 2015).
Rainfall changes and extreme events cause diverse effects on mammals, including changes in dominance patterns, local extinctions, mass mortality, reproductive failure, population booms, colonization by invasive species, and loss of functional diversity (Bateman et al., 2012, Lučan et al., 2013, Sherwin et al., 2013, Welbergen et al., 2008).
The tropics are extremely diverse and also increasingly under threat (Brown, 2014, Ceballos et al., 2007, Ceballos and Ehrlich, 2009, Rosenzweig, 1992). Tropical dry forests are threatened—and heavily managed—environments (Brown, 2014, Janzen, 1988, Rosenzweig, 1992, Stier and Mildenstein, 2005, Terborgh, 2013). Among the threats to these highly diverse habitats, recent studies point to extreme climate phenomena—particularly unusually strong hurricanes, higher temperatures, and longer droughts (IPCC, 2014, Mei et al., 2013, Milly et al., 2005, Seager et al., 2007).
The most diverse terrestrial ecosystems are the tropical forests, comprising over 60% of the mammal species on Earth (Brown, 2014). The most widely distributed are the tropical dry forests, which are seasonal ecosystems that depend on the precipitation and temperature patterns for their existence (Brown, 2014, Giam et al., 2012, Janzen, 1988, Rosenzweig, 1992). Although less exuberant than their tropical rain forests counterparts, tropical dry forests are extraordinarily rich, both in taxonomic and functional diversity, as well as in physiological and ecological strategies (Brown, 2014, Mason-Romo et al., 2017, Rosenzweig, 1992).
For extensive tropical dry-forest regions, international climate change models forecast reductions in precipitation of about 20% (IPCC, 2014). Thus, extreme climate phenomena have especially negative effects on tropical forests, where long-term data sets are particularly scarce (Cook et al., 2015, IPCC, 2014, Milly et al., 2005, Seager et al., 2007, Sheffield et al., 2012) and concrete predictions for species-specific impacts have hardly been addressed (Parmesan, 2006). Tropical forests are subject to extensive human activity, including forestry, animal grazing, clearing for agriculture, housing and development, causing a highly fragmented landscape (Quesada et al., 2009). To clearly separate the effects of climate from anthropogenic causes (such as poor management, intensive cattle grazing, and deforestation), studies must be conducted in well-preserved and protected habitats, which can function as refugia for biodiversity to recover after human-induced disturbances (Eigenbrod et al., 2015). Tropical species have also been documented to be more resilient than their non-tropical counterparts to climatic and anthropogenic disturbances (Moore and Huntington, 2008, Moritz and Agudo, 2013, Stork and Habel, 2014), but their resilience has been poorly studied in tropical dry forests.
Tropical dry forests in Western Mexico are seasonal ecosystems where rainfall (June to October) is the main driving factor of plant phenology and productivity (Anaya et al., 2012, Maass et al., 2005, Maass et al., 2002, Martínez-Yrizar et al., 1996). Primary productivity and temperature are known to be driving factors for the biodiversity in these ecosystems (Brown, 2014). One proxy for net primary productivity in deciduous forest is litterfall (Malhi et al., 2011), as it enables us to understand how much biomass was produced during the growing season. This remains true for the tropical dry forests because their very marked phenology can provide us with a precise measure of productivity throughout the year (Martínez-Yrízar et al. this issue). Most tropical dry forests are heavily populated and poorly managed by humans (Herrerías-Diego et al., 2006, Janzen, 1988, Miles et al., 2006). Such forests can be categorized as arroyo or upland. In the Chamela region in Jalisco, Mexico, arroyo forests (canopy height up to 25 m) are confined to lowlands and floodplains. Approximately 75% of the tree species in arroyo forests drop their foliage yearly, during the dry season (March to May). By contrast, upland forests occupy the far larger slopes and face dryer conditions. Trees are shorter (up to 15 m), and virtually all species remain leafless during dry season. These two ecosystems are found contiguously, but they differ in floristic composition and are phenologically contrasting (Anaya et al., 2012, Filip et al., 1995, Lott et al., 1987, Martínez-Yrizar et al., 1996, Palacios-Vargas et al., 2007).
The striking differences between these ecosystems and the populations inhabiting them are caused by processes we do not yet fully understand. Thus, it is pivotal to shed light on how the combined forces of intrinsic and extrinsic factors affect the long-term population dynamics of small mammals inhabiting these forests, how resilient these species are to such forces, and how will they perform in the projected global climate-disruption scenarios. Answering these questions is fundamental to properly manage and protect biodiversity and tropical forest ecosystems in the face of global climate disruption (Chapin et al., 2004, Chapin et al., 2000, Moritz and Agudo, 2013, Steneck et al., 2002, Stork et al., 2009, Zhou et al., 2013).
To answer those questions, we monitored the populations of seven native small mammals over an 18-year period in these two diverse and complex types of tropical dry forests. Through mathematical modeling of the species’ population dynamics, we assessed the influence of biotic factors (i.e., interactions within and between species and the influence of changes in net primary productivity) and abiotic factors (i.e., rainfall, temperature) in their population dynamics. We specifically addressed the following questions: (1) What are the effects of intrinsic (intraspecific) and extrinsic (interspecific interactions, temperature and rainfall and extreme climate events) factors on long-term population trends? (2) What are the implications of changes in these factors, such as the predicted changes in regional rainfall due to global climate disruption, for population dynamics and for forest conservation and management?
Section snippets
Study site
Data for this study were collected at Chamela-Cuixmala Biosphere Reserve (hereafter, Chamela), 19°30′ N, 105°03′ W, on Mexico’s western Pacific coast (S2). Chamela includes over 13,000 ha of well-preserved highly seasonal tropical dry forest landscape, with two contrasting forest types; upland and arroyo forests. Upland forest soils are relatively young and shallow (0.5–1 m depth), with tree height from 10 m to 15 m; over 95% of the tree species lose their leaves during the dry season. By
Species modeled
Our analyses included over 20,000 small mammal captures in both arroyo and upland forests (Fig. 1). Seven species accounted for 96% of all total captures: Liomys pictus (painted spiny pocket mouse), Nyctomys sumichrasti (vesper rat), Oryzomys melanotis (black-eared rice rat), Oryzomys mexicanus (Mexican rice rat), Osgoodomys banderanus (Michoacan deer mouse) and Peromyscus perfulvus (tawny deer mouse; Fig. 1). These species were abundant enough in the arroyo forest to be modeled (Figs. 1 and 2
Drivers of population dynamics
The population dynamics of this group of tropical dry forest mammals vary among species and between the two forest habitats (arroyo and upland). For most species, like some of their non-tropical counterparts, intrinsic factors are the basis of their dynamics (e.g., effects on cyclic dynamics of small mammals in northern Fennoscandia are intrinsic second-order effects of predation) (Aars and Ims, 2002, Hansen et al., 1999, Johannesen et al., 2003). This might suggest that their populations have
Acknowledgments
This paper is in partial fulfilment of the requirements for a PhD degree (EDMR) at the Posgrado en Ciencias Biológicas (PCBIOL), UNAM. Thanks to A. Farías, A. Gaxiola, A. Aguayo, A. Galicia, F. Jaksic, P. Sosenski, M. Alderete, P. Legendre, R. Dirzo, C. Rivera, S. Naeem, V. Sánchez-Cordero, C. and E. Vázquez for their valuable advice. Thanks to M. Healy and C. Brown, professional editors and friends, for their valuable revisions. Thanks to all those who helped in the long-term fieldwork and
References (131)
Basic and applied ecology functional web analysis: detecting the structure of population dynamics from multi-species time series
Basic Appl. Ecol.
(2001)- et al.
Inclusion of facilitation into ecological theory
Trends Ecol. Evol.
(2003) - et al.
Vive la difference: plant functional diversity matters to ecosystem processes: plant functional diversity matters to ecosystem processes
Trends Ecol. Evol.
(2001) - et al.
The relationship between solar radiation interception and soil water content in a tropical deciduous forest in Mexico
Catena
(1999) Biological consequences of global
Trends Ecol. Evol.
(2000)- et al.
Seasonal changes of leaf area index (LAI) in a tropical deciduous forest in west Mexico
For. Ecol. Manage.
(1995) - et al.
Biotic effects of climate change in urban environments: The case of the grey-headed flying-fox (Pteropus poliocephalus) in Melbourne, Australia
Biol. Conserv.
(2005) - et al.
Intrinsic and climatic determinants of population demography: the winter dynamics of tundra voles
Ecology
(2002) A new look at the statistical model identification
IEEE Trans. Autom. Control ACI
(1974)Information theory as an extension of the maximum likelihood principle
Large rainfall pulses control litter decomposition in a tropical dry forest: evidence from an 8-year study
Ecosystems
Geographical distributions of spiny pocket mice in South America: insights from predictive models
Glob. Ecol. Biogeogr.
Identifying refugia from climate change
J. Biogeogr.
Biotic interactions influence the projected distribution of a specialist mammal under climate change
Divers. Distrib.
On principles, laws and theory in population ecology
Oikos
On choosing models for describing and analyzing ecological time series
Ecology
Deciphering the effects of climate on animal populations:/rDiagnostic analysis provides new interpretation of/rSoay sheep dynamics
Am. Nat.
Climate extremes drive changes in functional community structure
Glob. Chang. Biol.
Why are there so many species in the tropics?
J. Biogeogr.
Species diversity of seed eating desert rodents in sand dune habitats
Ecology
Reorganization of an arid ecosystem in response to recent climate change
Proc. Natl. Acad. Sci. U. S. A.
Phenology of canopy trees of a tropical deciduous forest in Mexico
Biotropica
Comparative natural history of small mammals from tropical forests in Western Mexico
J. Mammal.
Rapid decline of a grassland system and its ecological and conservation implications
PLoS One
Discoveries of new mammal species and their implications for conservation and ecosystem services
Proc. Natl. Acad. Sci. U. S. A.
Global mammal distributions, biodiversity hotspots
Proc. Natl. Acad. Sci. U.S.A.
The sixth extinction crisis loss of animal populations and species
J. Cosmol.
Assessing conservation priorities in megadiverse Mexico: mammalian diversity, endemicity, and endangerment
Ecol. Appl.
Resilience and vulnerability of northern regions to social and environmental change
Ambio
Consequences of changing biodiversity
Nature
Unprecedented 21st century drought risk in the American Southwest and Central Plains
Sci. Adv.
Mammal population losses and the extinction crisis
Science (80.-)
Adult survival and population dynamics in the leaf-eared mouse Phyllotis darwini in central Chile
Rev. Chil. Hist. Nat.
Primary production dynamics and climate variability: Ecological consequences in semiarid Chile
Glob. Chang. Biol.
Defaunation in the Anthropocene
Science (80.-)
Vulnerability of ecosystems to climate change moderated by habitat intactness
Glob. Chang. Biol.
Long-term dynamics of voles and lemmings at the timberline and above the willow limit as a test of hypotheses on trophic interactions
Ecography (Cop.)
The Ten-Year Cycle in Numbers of the Lynx in Canada
J. Animal Ecol.
Periodic fluctuations in the numbers of animals: their causes and effects
Br. J. Exp. Biol.
Delayed density-dependent onset of spring reproduction in a fluctuating population of field voles
Oikos
Rodents, plants, and precipitation: spatial and temporal dynamics of consumers and resources
Oikos
Community assembly and invasion: an experimental test of neutral versus niche processes
Proc. Natl. Acad. Sci. U.S.A.
Within-year and among-year variation in the levels of herbivory on the foliage of trees from a Mexican tropical deciduous forest
Biotropica
Modificaciones al sistema de clasificación de Köppen
Biology of the Heteromyidae
Am. Soc. Mammalogists
Defaunation of tropical forests reduces habitat quality for seed-dispersing bats in Western Amazonia: An unexpected connection via mineral licks
Anim. Conserv.
Reservoirs of richness: least disturbed tropical forests are centres of undescribed species diversity
Proc. R. Soc. B Biol. Sci.
Projected Atlantic hurricane surge threat from rising temperatures
Proc. Natl. Acad. Sci. U. S. A.
Cited by (20)
Where could they go? Potential distribution of small mammals in the Caatinga under climate change scenarios
2024, Journal of Arid EnvironmentsMost Mexican hummingbirds lose under climate and land-use change: Long-term conservation implications
2021, Perspectives in Ecology and ConservationCitation Excerpt :This latter is noteworthy considering that more than three quarters of species showed a reduction of suitable habitat areas as a consequence of GCC. These results are in agreement with other studies in Mexico, not just for birds (Lara et al., 2012; Prieto-Torres et al., 2020, 2021a, 2021b) but for a wide variety of organisms, including mammals, amphibians, reptiles and plants (e.g., Ochoa-Ochoa et al., 2012; Sinervo et al., 2017; Mason-Romo et al., 2018; Ureta et al., 2018; Arenas-Navarro et al., 2020). These patterns of change are attributed to the expected increase in the average global temperature and decrease in the annual precipitation across the region (Cuervo-Robayo et al., 2020; Esperon-Rodriguez et al., 2019; Hidalgo, 2021), which could promote changes in the physiological responses and activity patterns of the biota.
Endemism of woody flora and tetrapod fauna, and conservation status of the inter-Andean Seasonally Dry Tropical Forest of the Marañón valley
2021, Global Ecology and ConservationCitation Excerpt :The aforementioned, demonstrates and highlights the need for research in this ecoregion compared to the ESDTF. The bird populations are highly dependent on the flora of the ISDTFM, as it is part of their diet (Roncal-Rabanal et al., 2020), which are constantly threatened by forest fragmentation, due to the expansion of the agricultural frontier and access roads (Chávez et al., 2021; Marcelo-Peña, 2017; Marcelo-Peña et al., 2010; Pennington and Muellner, 2010), which also affects the tetrapod fauna populations recorded in these forests. Likewise, these species could become extinct if hydroelectric, mining and oil projects located in the Marañón valley are implemented (Chávez et al., 2021; García-Bravo, 2011; Grandez et al., 2020).
Hygric Niches for Tropical Endotherms
2020, Trends in Ecology and EvolutionCitation Excerpt :Similarly, within a Mexican small mammal community, population growth rates varied in response to deviations in rainfall; five species increased in wetter years, while two were unaffected. Additionally, in response to extreme rainfall events, one species increased and three decreased [68]. The hygric niche framework predicts that population-level responses to temporal increases in rainfall should become consistently more negative in communities located in the wettest regions and, conversely, consistently more positive in communities located in the driest regions (Figure 2B).
Special Issue: Resilience of tropical dry forests to extreme disturbance events
2018, Forest Ecology and ManagementAssessing the vulnerability trifecta: species, climate, and anthropogenic pressures on protected areas of the Central Indian Highlands
2024, Journal of Wildlife Management
- ☆
This article is part of the Special Issue “Resilience of tropical dry forests to extreme disturbance events: An interdisciplinary perspective from long-term studies” published at the journal Forest Ecology and Management 426, 2018.