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1.  Tameness and stress physiology in a predator-naive island species confronted with novel predation threat 
Tame behaviour, i.e. low wariness, in terrestrial island species is often attributed to low predation pressure. However, we know little about its physiological control and its flexibility in the face of predator introductions. Marine iguanas (Amblyrhynchus cristatus) on the Galápagos Islands are a good model to study the physiological correlates of low wariness. They have lived virtually without predation for 5–15 Myr until some populations were first confronted with feral cats and dogs some 150 years ago. We tested whether and to what extent marine iguanas can adjust their behaviour and endocrine stress response to novel predation threats. Here, we show that a corticosterone stress response to experimental chasing is absent in naive animals, but is quickly restored with experience. Initially, low wariness also increases with experience, but remains an order of magnitude too low to allow successful escape from introduced predators. Our data suggest that the ability of marine iguanas to cope with predator introductions is limited by narrow reaction norms for behavioural wariness rather than by constraints in the underlying physiological stress system. In general, we predict that island endemics show flexible physiological stress responses but are restricted by narrow behavioural plasticity.
doi:10.1098/rspb.2006.3755
PMCID: PMC1766385  PMID: 17476779
anti-predator behaviour; wariness; corticosterone stress response; island endemic; introduced predator; Galápagos
2.  Phylogenetic analysis of the fecal microbial community in herbivorous land and marine iguanas of the Galápagos Islands using 16S rRNA-based pyrosequencing 
The ISME Journal  2011;5(9):1461-1470.
Herbivorous reptiles depend on complex gut microbial communities to effectively degrade dietary polysaccharides. The composition of these fermentative communities may vary based on dietary differences. To explore the role of diet in shaping gut microbial communities, we evaluated the fecal samples from two related host species—the algae-consuming marine iguana (Amblyrhynchus cristatus) and land iguanas (LI) (genus Conolophus) that consume terrestrial vegetation. Marine and LI fecal samples were collected from different islands in the Galápagos archipelago. High-throughput 16S rRNA-based pyrosequencing was used to provide a comparative analysis of fecal microbial diversity. At the phylum level, the fecal microbial community in iguanas was predominated by Firmicutes (69.5±7.9%) and Bacteroidetes (6.2±2.8%), as well as unclassified Bacteria (20.6±8.6%), suggesting that a large portion of iguana fecal microbiota is novel and could be involved in currently unknown functions. Host species differed in the abundance of specific bacterial groups. Bacteroides spp., Lachnospiraceae and Clostridiaceae were significantly more abundant in the marine iguanas (MI) (P-value>1E−9). In contrast, Ruminococcaceae were present at >5-fold higher abundance in the LI than MI (P-value>6E−14). Archaea were only detected in the LI. The number of operational taxonomic units (OTUs) in the LI (356–896 OTUs) was >2-fold higher than in the MI (112–567 OTUs), and this increase in OTU diversity could be related to the complexity of the resident bacterial population and their gene repertoire required to breakdown the recalcitrant polysaccharides prevalent in terrestrial plants. Our findings suggest that dietary differences contribute to gut microbial community differentiation in herbivorous lizards. Most importantly, this study provides a better understanding of the microbial diversity in the iguana gut; therefore facilitating future efforts to discover novel bacterial-associated enzymes that can effectively breakdown a wide variety of complex polysaccharides.
doi:10.1038/ismej.2011.33
PMCID: PMC3160690  PMID: 21451584
Galápagos iguanas; fecal microbiota; 16S rRNA-based pyrosequencing; dietary differences
3.  Stress physiology as a predictor of survival in Galapagos marine iguanas 
Although glucocorticoid hormones are considered important physiological regulators for surviving adverse environmental stimuli (stressors), evidence for such a role is sparse and usually extrapolated from glucocorticoid effects under laboratory, short-term and/or non-emergency conditions. Galápagos marine iguanas (Amblyrhynchus cristatus) provide an excellent model for determining the ultimate function of a glucocorticoid response because susceptibility to starvation induced by El Niño conditions is essentially their only major natural stressor. In a prospective study, we captured 98 adult male marine iguanas and assessed four major components of their glucocorticoid response: baseline corticosterone titres; corticosterone responses to acute stressors (capture and handling); the maximal capacity to secrete corticosterone (via adrenocorticotropin injection); and the ability to terminate corticosterone responses (negative feedback). Several months after collecting initial measurements, weak El Niño conditions affected the Galápagos and 23 iguanas died. The dead iguanas were typified by a reduced efficacy of negative feedback (i.e. poorer post-stress suppression of corticosterone release) compared with surviving iguanas. We found no prior differences between dead and alive iguanas in baseline corticosterone concentrations, responses to acute stressors, nor in capacity to respond. These data suggest that a greater ability to terminate a stress response conferred a survival advantage during starvation.
doi:10.1098/rspb.2010.0678
PMCID: PMC2982063  PMID: 20504812
stress; dexamethasone; adrenocorticotropin
4.  Progressive colonization and restricted gene flow shape island-dependent population structure in Galápagos marine iguanas (Amblyrhynchus cristatus) 
Background
Marine iguanas (Amblyrhynchus cristatus) inhabit the coastlines of large and small islands throughout the Galápagos archipelago, providing a rich system to study the spatial and temporal factors influencing the phylogeographic distribution and population structure of a species. Here, we analyze the microevolution of marine iguanas using the complete mitochondrial control region (CR) as well as 13 microsatellite loci representing more than 1200 individuals from 13 islands.
Results
CR data show that marine iguanas occupy three general clades: one that is widely distributed across the northern archipelago, and likely spread from east to west by way of the South Equatorial current, a second that is found mostly on the older eastern and central islands, and a third that is limited to the younger northern and western islands. Generally, the CR haplotype distribution pattern supports the colonization of the archipelago from the older, eastern islands to the younger, western islands. However, there are also signatures of recurrent, historical gene flow between islands after population establishment. Bayesian cluster analysis of microsatellite genotypes indicates the existence of twenty distinct genetic clusters generally following a one-cluster-per-island pattern. However, two well-differentiated clusters were found on the easternmost island of San Cristóbal, while nine distinct and highly intermixed clusters were found on youngest, westernmost islands of Isabela and Fernandina. High mtDNA and microsatellite genetic diversity were observed for populations on Isabela and Fernandina that may be the result of a recent population expansion and founder events from multiple sources.
Conclusions
While a past genetic study based on pure FST analysis suggested that marine iguana populations display high levels of nuclear (but not mitochondrial) gene flow due to male-biased dispersal, the results of our sex-biased dispersal tests and the finding of strong genetic differentiation between islands do not support this view. Therefore, our study is a nice example of how recently developed analytical tools such as Bayesian clustering analysis and DNA sequence-based demographic analyses can overcome potential biases introduced by simply relying on FST estimates from markers with different inheritance patterns.
doi:10.1186/1471-2148-9-297
PMCID: PMC2807874  PMID: 20028547
5.  Coping with continuous human disturbance in the wild: insights from penguin heart rate response to various stressors 
BMC Ecology  2012;12:10.
Background
A central question for ecologists is the extent to which anthropogenic disturbances (e.g. tourism) might impact wildlife and affect the systems under study. From a research perspective, identifying the effects of human disturbance caused by research-related activities is crucial in order to understand and account for potential biases and derive appropriate conclusions from the data.
Results
Here, we document a case of biological adjustment to chronic human disturbance in a colonial seabird, the king penguin (Aptenodytes patagonicus), breeding on remote and protected islands of the Southern ocean. Using heart rate (HR) as a measure of the stress response, we show that, in a colony with areas exposed to the continuous presence of humans (including scientists) for over 50 years, penguins have adjusted to human disturbance and habituated to certain, but not all, types of stressors. When compared to birds breeding in relatively undisturbed areas, birds in areas of high chronic human disturbance were found to exhibit attenuated HR responses to acute anthropogenic stressors of low-intensity (i.e. sounds or human approaches) to which they had been subjected intensely over the years. However, such attenuation was not apparent for high-intensity stressors (i.e. captures for scientific research) which only a few individuals experience each year.
Conclusions
Habituation to anthropogenic sounds/approaches could be an adaptation to deal with chronic innocuous stressors, and beneficial from a research perspective. Alternately, whether penguins have actually habituated to anthropogenic disturbances over time or whether human presence has driven the directional selection of human-tolerant phenotypes, remains an open question with profound ecological and conservation implications, and emphasizes the need for more knowledge on the effects of human disturbance on long-term studied populations.
doi:10.1186/1472-6785-12-10
PMCID: PMC3543187  PMID: 22784366
Stress; Heart rate; Habituation; Selection; Seabird; Human disturbance; Long-term monitoring
6.  Ape Conservation Physiology: Fecal Glucocorticoid Responses in Wild Pongo pygmaeus morio following Human Visitation 
PLoS ONE  2012;7(3):e33357.
Nature-based tourism can generate important revenue to support conservation of biodiversity. However, constant exposure to tourists and subsequent chronic activation of stress responses can produce pathological effects, including impaired cognition, growth, reproduction, and immunity in the same animals we are interested in protecting. Utilizing fecal samples (N = 53) from 2 wild habituated orangutans (Pongo pygmaeus morio) (in addition to 26 fecal samples from 4 wild unhabituated orangutans) in the Lower Kinabatangan Wildlife Sanctuary of Sabah, Malaysian Borneo, we predicted that i) fecal glucocorticoid metabolite concentrations would be elevated on the day after tourist visitation (indicative of normal stress response to exposure to tourists on the previous day) compared to samples taken before or during tourist visitation in wild, habituated orangutans, and ii) that samples collected from habituated animals would have lower fecal glucocorticoid metabolites than unhabituated animals not used for tourism. Among the habituated animals used for tourism, fecal glucocorticoid metabolite levels were significantly elevated in samples collected the day after tourist visitation (indicative of elevated cortisol production on the previous day during tourist visitation). Fecal glucocorticoid metabolite levels were also lower in the habituated animals compared to their age-matched unhabituated counterparts. We conclude that the habituated animals used for this singular ecotourism project are not chronically stressed, unlike other species/populations with documented permanent alterations in stress responses. Animal temperament, species, the presence of coping/escape mechanisms, social confounders, and variation in amount of tourism may explain differences among previous experiments. Acute alterations in glucocorticoid measures in wildlife exposed to tourism must be interpreted conservatively. While permanently altered stress responses can be detrimental, preliminary results in these wild habituated orangutans suggest that low levels of predictable disturbance can likely result in low physiological impact on these animals.
doi:10.1371/journal.pone.0033357
PMCID: PMC3305311  PMID: 22438916
7.  Population, Behavioural and Physiological Responses of an Urban Population of Black Swans to an Intense Annual Noise Event 
PLoS ONE  2012;7(9):e45014.
Wild animals in urban environments are exposed to a broad range of human activities that have the potential to disturb their life history and behaviour. Wildlife responses to disturbance can range from emigration to modified behaviour, or elevated stress, but these responses are rarely evaluated in concert. We simultaneously examined population, behavioural and hormonal responses of an urban population of black swans Cygnus atratus before, during and after an annual disturbance event involving large crowds and intense noise, the Australian Formula One Grand Prix. Black swan population numbers were lowest one week before the event and rose gradually over the course of the study, peaking after the event, suggesting that the disturbance does not trigger mass emigration. We also found no difference in the proportion of time spent on key behaviours such as locomotion, foraging, resting or self-maintenance over the course of the study. However, basal and capture stress-induced corticosterone levels showed significant variation, consistent with a modest physiological response. Basal plasma corticosterone levels were highest before the event and decreased over the course of the study. Capture-induced stress levels peaked during the Grand Prix and then also declined over the remainder of the study. Our results suggest that even intensely noisy and apparently disruptive events may have relatively low measurable short-term impact on population numbers, behaviour or physiology in urban populations with apparently high tolerance to anthropogenic disturbance. Nevertheless, the potential long-term impact of such disturbance on reproductive success, individual fitness and population health will need to be carefully evaluated.
doi:10.1371/journal.pone.0045014
PMCID: PMC3443219  PMID: 23024783
8.  Spatial Analysis of Factors Influencing Long-Term Stress in the Grizzly Bear (Ursus arctos) Population of Alberta, Canada 
PLoS ONE  2013;8(12):e83768.
Non-invasive measures for assessing long-term stress in free ranging mammals are an increasingly important approach for understanding physiological responses to landscape conditions. Using a spatially and temporally expansive dataset of hair cortisol concentrations (HCC) generated from a threatened grizzly bear (Ursus arctos) population in Alberta, Canada, we quantified how variables representing habitat conditions and anthropogenic disturbance impact long-term stress in grizzly bears. We characterized spatial variability in male and female HCC point data using kernel density estimation and quantified variable influence on spatial patterns of male and female HCC stress surfaces using random forests. Separate models were developed for regions inside and outside of parks and protected areas to account for substantial differences in anthropogenic activity and disturbance within the study area. Variance explained in the random forest models ranged from 55.34% to 74.96% for males and 58.15% to 68.46% for females. Predicted HCC levels were higher for females compared to males. Generally, high spatially continuous female HCC levels were associated with parks and protected areas while low-to-moderate levels were associated with increased anthropogenic disturbance. In contrast, male HCC levels were low in parks and protected areas and low-to-moderate in areas with increased anthropogenic disturbance. Spatial variability in gender-specific HCC levels reveal that the type and intensity of external stressors are not uniform across the landscape and that male and female grizzly bears may be exposed to, or perceive, potential stressors differently. We suggest observed spatial patterns of long-term stress may be the result of the availability and distribution of foods related to disturbance features, potential sexual segregation in available habitat selection, and may not be influenced by sources of mortality which represent acute traumas. In this wildlife system and others, conservation and management efforts can benefit by understanding spatial- and gender-based stress responses to landscape conditions.
doi:10.1371/journal.pone.0083768
PMCID: PMC3873976  PMID: 24386273
9.  Emulating Natural Disturbances for Declining Late-Successional Species: A Case Study of the Consequences for Cerulean Warblers (Setophaga cerulea) 
PLoS ONE  2013;8(1):e52107.
Forest cover in the eastern United States has increased over the past century and while some late-successional species have benefited from this process as expected, others have experienced population declines. These declines may be in part related to contemporary reductions in small-scale forest interior disturbances such as fire, windthrow, and treefalls. To mitigate the negative impacts of disturbance alteration and suppression on some late-successional species, strategies that emulate natural disturbance regimes are often advocated, but large-scale evaluations of these practices are rare. Here, we assessed the consequences of experimental disturbance (using partial timber harvest) on a severely declining late-successional species, the cerulean warbler (Setophaga cerulea), across the core of its breeding range in the Appalachian Mountains. We measured numerical (density), physiological (body condition), and demographic (age structure and reproduction) responses to three levels of disturbance and explored the potential impacts of disturbance on source-sink dynamics. Breeding densities of warblers increased one to four years after all canopy disturbances (vs. controls) and males occupying territories on treatment plots were in better condition than those on control plots. However, these beneficial effects of disturbance did not correspond to improvements in reproduction; nest success was lower on all treatment plots than on control plots in the southern region and marginally lower on light disturbance plots in the northern region. Our data suggest that only habitats in the southern region acted as sources, and interior disturbances in this region have the potential to create ecological traps at a local scale, but sources when viewed at broader scales. Thus, cerulean warblers would likely benefit from management that strikes a landscape-level balance between emulating natural disturbances in order to attract individuals into areas where current structure is inappropriate, and limiting anthropogenic disturbance in forests that already possess appropriate structural attributes in order to maintain maximum productivity.
doi:10.1371/journal.pone.0052107
PMCID: PMC3537674  PMID: 23308104
10.  A western gray whale mitigation and monitoring program for a 3-D seismic survey, Sakhalin Island, Russia 
The introduction of anthropogenic sounds into the marine environment can impact some marine mammals. Impacts can be greatly reduced if appropriate mitigation measures and monitoring are implemented. This paper concerns such measures undertaken by Exxon Neftegas Limited, as operator of the Sakhalin-1 Consortium, during the Odoptu 3-D seismic survey conducted during 17 August’ September 2001. The key environmental issue was protection of the critically endangered western gray whale (Eschrichtius robustus), which feeds in summer and fall primarily in the Piltun feeding area off northeast Sakhalin Island. Existing mitigation and monitoring practices for seismic surveys in other jurisdictions were evaluated to identify best practices for reducing impacts on feeding activity by western gray whales. Two buffer zones were established to protect whales from physical injury or undue disturbance during feeding. A 1 km buffer protected all whales from exposure to levels of sound energy potentially capable of producing physical injury. A 4’ km buffer was established to avoid displacing western gray whales from feeding areas. Trained Marine Mammal Observers (MMOs) on the seismic ship Nordic Explorer had the authority to shut down the air guns if whales were sighted within these buffers.
Additional mitigation measures were also incorporated: Temporal mitigation was provided by rescheduling the program from June–August to August–September to avoid interference with spring arrival of migrating gray whales. The survey area was reduced by 19% to avoid certain waters <20 m deep where feeding whales concentrated and where seismic acquisition was a lower priority. The number of air guns and total volume of the air guns were reduced by about half (from 28 to 14 air guns and from 3,390 in3 to 1,640 in3) relative to initial plans. ‘Ramp-up’(=‘soft-start’ procedures were implemented.
Monitoring activities were conducted as needed to implement some mitigation measures, and to assess residual impacts. Aerial and vessel-based surveys determined the distribution of whales before, during and after the seismic survey. Daily aerial reconnaissance helped verify whale-free areas and select the sequence of seismic lines to be surveyed. A scout vessel with MMOs aboard was positioned 4 km shoreward of the active seismic vessel to provide better visual coverage of the 4’ km buffer and to help define the inshore edge of the 4’ km buffer. A second scout vessel remained near the seismic vessel. Shore-based observers determined whale numbers, distribution, and behavior during and after the seismic survey. Acoustic monitoring documented received sound levels near and in the main whale feeding area.
Statistical analyses of aerial survey data indicated that about 5’0 gray whales moved away from waters near (inshore of) the seismic survey during seismic operations. They shifted into the core gray whale feeding area farther south, and the proportion of gray whales observed feeding did not change over the study period.
Five shutdowns of the air guns were invoked for gray whales seen within or near the buffer. A previously unknown gray whale feeding area (the Offshore feeding area) was discovered south and offshore from the nearshore Piltun feeding area. The Offshore area has subsequently been shown to be used by feeding gray whales during several years when no anthropogenic activity occurred near the Piltun feeding area.
Shore-based counts indicated that whales continued to feed inshore of the Odoptu block throughout the seismic survey, with no significant correlation between gray whale abundance and seismic activity. Average values of most behavioral parameters were similar to those without seismic surveys. Univariate analysis showed no correlation between seismic sound levels and any behavioral parameter. Multiple regression analyses indicated that, after allowance for environmental covariates, 5 of 11 behavioral parameters were statistically correlated with estimated seismic survey-related variables; 6 of 11 behavioral parameters were not statistically correlated with seismic survey-related variables. Behavioral parameters that were correlated with seismic variables were transient and within the range of variation attributable to environmental effects.
Acoustic monitoring determined that the 4’ km buffer zone, in conjunction with reduction of the air gun array to 14 guns and 1,640 in3, was effective in limiting sound exposure. Within the Piltun feeding area, these mitigation measures were designed to insure that western gray whales were not exposed to received levels exceeding the 163 dB re 1 μPa (rms) threshold.
This was among the most complex and intensive mitigation programs ever conducted for any marine mammal. It provided valuable new information about underwater sounds and gray whale responses during a nearshore seismic program that will be useful in planning future work. Overall, the efforts in 2001 were successful in reducing impacts to levels tolerable by western gray whales. Research in 2002’005 suggested no biologically significant or population-level impacts of the 2001 seismic survey.
doi:10.1007/s10661-007-9813-0
PMCID: PMC2798040  PMID: 17657576
Seismic survey; Mitigation; Monitoring; Western gray whale; Eschrichtius robustus; Sakhalin Island; Okhotsk Sea; Russia
11.  Genetic Impact of a Severe El Niño Event on Galápagos Marine Iguanas (Amblyrhynchus cristatus) 
PLoS ONE  2007;2(12):e1285.
The El Niño-Southern Oscillation (ENSO) is a major source of climatic disturbance, impacting the dynamics of ecosystems worldwide. Recent models predict that human-generated rises in green-house gas levels will cause an increase in the strength and frequency of El Niño warming events in the next several decades, highlighting the need to understand the potential biological consequences of increased ENSO activity. Studies have focused on the ecological and demographic implications of El Niño in a range of organisms, but there have been few systematic attempts to measure the impact of these processes on genetic diversity in populations. Here, we evaluate whether the 1997–1998 El Niño altered the genetic composition of Galápagos marine iguana populations from eleven islands, some of which experienced mortality rates of up to 90% as a result of El Niño warming. Specifically, we measured the temporal variation in microsatellite allele frequencies and mitochondrial DNA diversity (mtDNA) in samples collected before (1991/1993) and after (2004) the El Niño event. Based on microsatellite data, only one island (Marchena) showed signatures of a genetic bottleneck, where the harmonic mean of the effective population size (Ne) was estimated to be less than 50 individuals during the period between samplings. Substantial decreases in mtDNA variation between time points were observed in populations from just two islands (Marchena and Genovesa). Our results suggests that, for the majority of islands, a single, intense El Niño event did not reduce marine iguana populations to the point where substantial neutral genetic diversity was lost. In the case of Marchena, simultaneous changes to both nuclear and mitochondrial DNA variation may also be the result of a volcanic eruption on the island in 1991. Therefore, studies that seek to evaluate the genetic impact of El Niño must also consider the confounding or potentially synergistic effect of other environmental and biological forces shaping populations.
doi:10.1371/journal.pone.0001285
PMCID: PMC2110882  PMID: 18074011
12.  Logging Affects Fledgling Sex Ratios and Baseline Corticosterone in a Forest Songbird 
PLoS ONE  2012;7(3):e33124.
Silviculture (logging) creates a disturbance to forested environments. The degree to which forests are modified depends on the logging prescription and forest stand characteristics. In this study we compared the effects of two methods of group-selection (“moderate” and “heavy”) silviculture (GSS) and undisturbed reference stands on stress and offspring sex ratios of a forest interior species, the Ovenbird (Seiurus aurocapilla), in Algonquin Provincial Park, Canada. Blood samples were taken from nestlings for corticosterone and molecular sexing. We found that logging creates a disturbance that is stressful for nestling Ovenbirds, as illustrated by elevated baseline corticosterone in cut sites. Ovenbirds nesting in undisturbed reference forest produce fewer male offspring per brood (proportion male = 30%) while logging with progressively greater forest disturbance, shifted the offspring sex ratio towards males (proportion male: moderate = 50%, heavy = 70%). If Ovenbirds in undisturbed forests usually produce female-biased broods, then the production of males as a result of logging may disrupt population viability. We recommend a broad examination of nestling sex ratios in response to anthropogenic disturbance to determine the generality of our findings.
doi:10.1371/journal.pone.0033124
PMCID: PMC3303809  PMID: 22432000
13.  Effects of social disruption in elephants persist decades after culling 
Frontiers in Zoology  2013;10:62.
Background
Multi-level fission-fusion societies, characteristic of a number of large brained mammal species including some primates, cetaceans and elephants, are among the most complex and cognitively demanding animal social systems. Many free-ranging populations of these highly social mammals already face severe human disturbance, which is set to accelerate with projected anthropogenic environmental change. Despite this, our understanding of how such disruption affects core aspects of social functioning is still very limited.
Results
We now use novel playback experiments to assess decision-making abilities integral to operating successfully within complex societies, and provide the first systematic evidence that fundamental social skills may be significantly impaired by anthropogenic disruption. African elephants (Loxodonta africana) that had experienced separation from family members and translocation during culling operations decades previously performed poorly on systematic tests of their social knowledge, failing to distinguish between callers on the basis of social familiarity. Moreover, elephants from the disrupted population showed no evidence of discriminating between callers when age-related cues simulated individuals on an increasing scale of social dominance, in sharp contrast to the undisturbed population where this core social ability was well developed.
Conclusions
Key decision-making abilities that are fundamental to living in complex societies could be significantly altered in the long-term through exposure to severely disruptive events (e.g. culling and translocation). There is an assumption that wildlife responds to increasing pressure from human societies only in terms of demography, however our study demonstrates that the effects may be considerably more pervasive. These findings highlight the potential long-term negative consequences of acute social disruption in cognitively advanced species that live in close-knit kin-based societies, and alter our perspective on the health and functioning of populations that have been subjected to anthropogenic disturbance.
doi:10.1186/1742-9994-10-62
PMCID: PMC3874604  PMID: 24152378
Social behaviour; Human disturbance; Anthropogenic disruption; Cognitive abilities; Playback experiment; Large-brained mammals; Social organisation; Loxodonta africana; Fission-fusion society; Vocal communication; Matriarch
14.  Human Disturbance Influences Reproductive Success and Growth Rate in California Sea Lions (Zalophus californianus) 
PLoS ONE  2011;6(3):e17686.
The environment is currently undergoing changes at both global (e.g., climate change) and local (e.g., tourism, pollution, habitat modification) scales that have the capacity to affect the viability of animal and plant populations. Many of these changes, such as human disturbance, have an anthropogenic origin and therefore may be mitigated by management action. To do so requires an understanding of the impact of human activities and changing environmental conditions on population dynamics. We investigated the influence of human activity on important life history parameters (reproductive rate, and body condition, and growth rate of neonate pups) for California sea lions (Zalophus californianus) in the Gulf of California, Mexico. Increased human presence was associated with lower reproductive rates, which translated into reduced long-term population growth rates and suggested that human activities are a disturbance that could lead to population declines. We also observed higher body growth rates in pups with increased exposure to humans. Increased growth rates in pups may reflect a density dependent response to declining reproductive rates (e.g., decreased competition for resources). Our results highlight the potentially complex changes in life history parameters that may result from human disturbance, and their implication for population dynamics. We recommend careful monitoring of human activities in the Gulf of California and emphasize the importance of management strategies that explicitly consider the potential impact of human activities such as ecotourism on vertebrate populations.
doi:10.1371/journal.pone.0017686
PMCID: PMC3059216  PMID: 21436887
15.  Is coral richness related to community resistance to and recovery from disturbance? 
PeerJ  2014;2:e308.
More diverse communities are thought to be more stable—the diversity–stability hypothesis—due to increased resistance to and recovery from disturbances. For example, high diversity can make the presence of resilient or fast growing species and key facilitations among species more likely. How natural, geographic biodiversity patterns and changes in biodiversity due to human activities mediate community-level disturbance dynamics is largely unknown, especially in diverse systems. For example, few studies have explored the role of diversity in tropical marine communities, especially at large scales. We tested the diversity–stability hypothesis by asking whether coral richness is related to resistance to and recovery from disturbances including storms, predator outbreaks, and coral bleaching on tropical coral reefs. We synthesized the results of 41 field studies conducted on 82 reefs, documenting changes in coral cover due to disturbance, across a global gradient of coral richness. Our results indicate that coral reefs in more species-rich regions were marginally less resistant to disturbance and did not recover more quickly. Coral community resistance was also highly dependent on pre-disturbance coral cover, probably due in part to the sensitivity of fast-growing and often dominant plating acroporid corals to disturbance. Our results suggest that coral communities in biodiverse regions, such as the western Pacific, may not be more resistant and resilient to natural and anthropogenic disturbances. Further analyses controlling for disturbance intensity and other drivers of coral loss and recovery could improve our understanding of the influence of diversity on community stability in coral reef ecosystems.
doi:10.7717/peerj.308
PMCID: PMC3970800  PMID: 24711964
Biodiveristy; Resilience; Stability; Coral reef; Disturbance; Recovery; Resistance; Community ecology
16.  Spreading free-riding snow sports represent a novel serious threat for wildlife 
Stress generated by humans on wildlife by continuous development of outdoor recreational activities is of increasing concern for biodiversity conservation. Human disturbance often adds to other negative impact factors affecting the dynamics of vulnerable populations. It is not known to which extent the rapidly spreading free-riding snow sports actually elicit detrimental stress (allostatic overload) upon wildlife, nor what the potential associated fitness and survival costs are. Using a non-invasive technique, we evaluated the physiological stress response induced by free-riding snow sports on a declining bird species of Alpine ecosystems. The results of a field experiment in which radiomonitored black grouse (Tetrao tetrix) were actively flushed from their snow burrows once a day during four consecutive days showed an increase in the concentration of faecal stress hormone (corticosterone) metabolites after disturbance. A large-scale comparative analysis across the southwestern Swiss Alps indicated that birds had higher levels of these metabolites in human-disturbed versus undisturbed habitats. Disturbance by snow sport free-riders appears to elevate stress, which potentially represents a new serious threat for wildlife. The fitness and survival costs of allostatic adjustments have yet to be estimated.
doi:10.1098/rspb.2006.0434
PMCID: PMC2189568  PMID: 17341459
stress ecology; conservation biology; species protection; alpine ecosystems; human disturbance; winter snow sports
17.  Evolution of body size in Galapagos marine iguanas 
Body size is one of the most important traits of organisms and allows predictions of an individual's morphology, physiology, behaviour and life history. However, explaining the evolution of complex traits such as body size is difficult because a plethora of other traits influence body size. Here I review what we know about the evolution of body size in a group of island reptiles and try to generalize about the mechanisms that shape body size. Galapagos marine iguanas occupy all 13 larger islands in this Pacific archipelago and have maximum island body weights between 900 and 12 000 g. The distribution of body sizes does not match mitochondrial clades, indicating that body size evolves independently of genetic relatedness. Marine iguanas lack intra- and inter-specific food competition and predators are not size-specific, discounting these factors as selective agents influencing body size. Instead I hypothesize that body size reflects the trade-offs between sexual and natural selection. We found that sexual selection continuously favours larger body sizes. Large males establish display territories and some gain over-proportional reproductive success in the iguanas' mating aggregations. Females select males based on size and activity and are thus responsible for the observed mating skew. However, large individuals are strongly selected against during El Niño-related famines when dietary algae disappear from the intertidal foraging areas. We showed that differences in algae sward (‘pasture’) heights and thermal constraints on large size are causally responsible for differences in maximum body size among populations. I hypothesize that body size in many animal species reflects a trade-off between foraging constraints and sexual selection and suggest that future research could focus on physiological and genetic mechanisms determining body size in wild animals. Furthermore, evolutionary stable body size distributions within populations should be analysed to better understand selection pressures on individual body size.
doi:10.1098/rspb.2005.3205
PMCID: PMC1559900  PMID: 16191607
reptile; scaling; digestion; thermoregulation; diving; island rule
18.  Heterospecific alarm call recognition in a non-vocal reptile 
Biology Letters  2007;3(6):632-634.
The ability to recognize and respond to the alarm calls of heterospecifics has previously been described only in species with vocal communication. Here we provide evidence that a non-vocal reptile, the Galápagos marine iguana (Amblyrhynchus cristatus), can eavesdrop on the alarm call of the Galápagos mockingbird (Nesomimus parvulus) and respond with anti-predator behaviour. Eavesdropping on complex heterospecific communications demonstrates a remarkable degree of auditory discrimination in a non-vocal species.
doi:10.1098/rsbl.2007.0443
PMCID: PMC2391237  PMID: 17911047
eavesdropping; heterospecific recognition; animal communication; marine iguanas
19.  Anthropogenic Disturbance and Biodiversity of Marine Benthic Communities in Antarctica: A Regional Comparison 
PLoS ONE  2014;9(6):e98802.
The impacts of two Antarctic stations in different regions, on marine sediment macrofaunal communities were compared: McMurdo, a very large station in the Ross Sea; and Casey, a more typical small station in East Antarctica. Community structure and diversity were compared along a gradient of anthropogenic disturbance from heavily contaminated to uncontaminated locations. We examined some of the inherent problems in comparing data from unrelated studies, such as different sampling methods, spatial and temporal scales of sampling and taxonomic uncertainty. These issues generated specific biases which were taken into account when interpreting patterns. Control sites in the two regions had very different communities but both were dominated by crustaceans. Community responses to anthropogenic disturbance (sediment contamination by metals, oils and sewage) were also different. At McMurdo the proportion of crustaceans decreased in disturbed areas and polychaetes became dominant, whereas at Casey, crustaceans increased in response to disturbance, largely through an increase in amphipods. Despite differing overall community responses there were some common elements. Ostracods, cumaceans and echinoderms were sensitive to disturbance in both regions. Capitellid, dorvelleid and orbiniid polychaetes were indicative of disturbed sites. Amphipods, isopods and tanaids had different responses at each station. Biodiversity and taxonomic distinctness were significantly lower at disturbed locations in both regions. The size of the impact, however, was not related to the level of contamination, with a larger reduction in biodiversity at Casey, the smaller, less polluted station. The impacts of small stations, with low to moderate levels of contamination, can thus be as great as those of large or heavily contaminated stations. Regional broad scale environmental influences may be important in determining the composition of communities and thus their response to disturbance, but there are some generalizations regarding responses which will aid future management of stations.
doi:10.1371/journal.pone.0098802
PMCID: PMC4053418  PMID: 24919053
20.  A specialist-generalist classification of the arable flora and its response to changes in agricultural practices 
BMC Ecology  2010;10:20.
Background
Theory in ecology points out the potential link between the degree of specialisation of organisms and their responses to disturbances and suggests that this could be a key element for understanding the assembly of communities. We evaluated this question for the arable weed flora as this group has scarcely been the focus of ecological studies so far and because weeds are restricted to habitats characterised by very high degrees of disturbance. As such, weeds offer a case study to ask how specialization relates to abundance and distribution of species in relation to the varying disturbance regimes occurring in arable crops.
Results
We used data derived from an extensive national monitoring network of approximately 700 arable fields scattered across France to quantify the degree of specialisation of 152 weed species using six different ecological methods. We then explored the impact of the level of disturbance occurring in arable fields by comparing the degree of specialisation of weed communities in contrasting field situations.
The classification of species as specialist or generalist was consistent between different ecological indices. When applied on a large-scale data set across France, this classification highlighted that monoculture harbour significantly more specialists than crop rotations, suggesting that crop rotation increases abundance of generalist species rather than sets of species that are each specialised to the individual crop types grown in the rotation. Applied to a diachronic dataset, the classification also shows that the proportion of specialist weed species has significantly decreased in cultivated fields over the last 30 years which suggests a biotic homogenization of agricultural landscapes.
Conclusions
This study shows that the concept of generalist/specialist species is particularly relevant to understand the effect of anthropogenic disturbances on the evolution of plant community composition and that ecological theories developed in stable environments are valid in highly disturbed environments such as agro-ecosystems. The approach developed here to classify arable weeds according to the breadth of their ecological niche is robust and applicable to a wide range of organisms. It is also sensitive to disturbance regime and we show here that recent changes in agricultural practices, i.e. increased levels of disturbance have favoured the most generalist species, hence leading to biotic homogenisation in arable landscapes.
doi:10.1186/1472-6785-10-20
PMCID: PMC2939635  PMID: 20809982
21.  16SrDNA Pyrosequencing of the Mediterranean Gorgonian Paramuricea clavata Reveals a Link among Alterations in Bacterial Holobiont Members, Anthropogenic Influence and Disease Outbreaks 
PLoS ONE  2013;8(6):e67745.
Mass mortality events of benthic invertebrates in the Mediterranean Sea are becoming an increasing concern with catastrophic effects on the coastal marine environment. Sea surface temperature anomalies leading to physiological stress, starvation and microbial infections were identified as major factors triggering animal mortality. However the highest occurrence of mortality episodes in particular geographic areas and occasionally in low temperature deep environments suggest that other factors play a role as well. We conducted a comparative analysis of bacterial communities associated with the purple gorgonian Paramuricea clavata, one of the most affected species, collected at different geographic locations and depth, showing contrasting levels of anthropogenic disturbance and health status. Using massive parallel 16SrDNA gene pyrosequencing we showed that the bacterial community associated with healthy P. clavata in pristine locations was dominated by a single genus Endozoicomonas within the order Oceanospirillales which represented ∼90% of the overall bacterial community. P. clavata samples collected in human impacted areas and during disease events had higher bacterial diversity and abundance of disease-related bacteria, such as vibrios, than samples collected in pristine locations whilst showed a reduced dominance of Endozoicomonas spp. In contrast, bacterial symbionts exhibited remarkable stability in P. clavata collected both at euphotic and mesophotic depths in pristine locations suggesting that fluctuations in environmental parameters such as temperature have limited effect in structuring the bacterial holobiont. Interestingly the coral pathogen Vibrio coralliilyticus was not found on diseased corals collected during a deep mortality episode suggesting that neither temperature anomalies nor recognized microbial pathogens are solely sufficient to explain for the events. Overall our data suggest that anthropogenic influence may play a significant role in determining the coral health status by affecting the composition of the associated microbial community. Environmental stressful events and microbial infections may thus be superimposed to compromise immunity and trigger mortality outbreaks.
doi:10.1371/journal.pone.0067745
PMCID: PMC3694090  PMID: 23840768
22.  Human-induced morphological shifts in an island lizard 
Evolutionary Applications  2011;4(2):388-396.
Understanding the evolutionary consequences of anthropogenic change is an emerging topic in evolutionary biology. While highly sensitive species may go extinct in response to anthropogenic habitat alteration, those with broader environmental tolerances may persist and adapt to the changes. Here, we use morphological data from the brown anole (Anolis sagrei), a lizard species that lives in both natural and human-disturbed habitats, to examine the impact of anthropogenic habitat alteration. We find populations inhabiting disturbed habitats were significantly larger in snout-vent length, hindspan, and mass and provide evidence that the observed divergence in hindspan is driven by human-induced changes in habitat structure. Populations were found to be genetically distinct among islands but are not genetically differentiated between habitat types on islands. Thus, the observed pattern of intra-island morphological differences cannot be explained by separate founding populations. Rather, our results are consistent with morphological differences between habitats having arisen in situ on each island. Results underscore the significant impact anthropogenic change may have on evolutionary trajectories of populations that persist in human-altered habitats.
doi:10.1111/j.1752-4571.2010.00170.x
PMCID: PMC3352549
Anolis lizards; anthropogenic change; habitat structure; island; selection
23.  Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas 
Hormones and behavior  2008;55(2):329-337.
Our aim was to identify natural and anthropogenic influences on the stress physiology of large African carnivores, using wild spotted hyenas (Crocuta crocuta) as model animals. With both longitudinal data from a single social group, and cross-sectional data from multiple groups, we used fecal glucocorticoids (fGC) to examine potential stressors among spotted hyenas. Longitudinal data from adult members of a group living on the edge of the Masai Mara National Reserve, Kenya, revealed that fGC concentrations were elevated during two periods of social upheaval among adults, especially among younger females; however, prey availability, rainfall, and presence of lions did not influence fGC concentrations among hyenas. Our results suggested that anthropogenic disturbance in the form of pastoralist activity, but not tourism, influenced fGC concentrations among adult male hyenas; rising concentrations of fGC among males over 12 years were significantly correlated with increasing human population density along the edge of the group’s home range. As hyenas from this social group were frequently exposed to anthropogenic disturbance, we compared fGC concentrations among these hyenas with those obtained concurrently from hyenas living in three other groups undisturbed by pastoralist activity. We found that fGC concentrations from the undisturbed groups were significantly lower than those in the disturbed group, and we were able to rule out tourism and ecological stressors as sources of variation in fGC among the populations. Thus it appears that both social instability and anthropogenic disturbance, but not the ecological variables examined, elevate fGC concentrations and represent stressors for wild spotted hyenas. Further work will be necessary to determine whether interpopulation variation in stress physiology predicts population decline in groups exposed to intensive anthropogenic disturbance.
doi:10.1016/j.yhbeh.2008.11.001
PMCID: PMC2987620  PMID: 19056392
Crocuta; Glucocorticoids; Stress; Anthropogenic disturbance
24.  Immune Activity, Body Condition and Human-Associated Environmental Impacts in a Wild Marine Mammal 
PLoS ONE  2013;8(6):e67132.
Within individuals, immunity may compete with other life history traits for resources, such as energy and protein, and the damage caused by immunopathology can sometimes outweigh the protective benefits that immune responses confer. However, our understanding of the costs of immunity in the wild and how they relate to the myriad energetic demands on free-ranging organisms is limited. The endangered Galapagos sea lion (Zalophus wollebaeki) is threatened simultaneously by disease from domestic animals and rapid changes in food availability driven by unpredictable environmental variation. We made use of this unique ecology to investigate the relationship between changes in immune activity and changes in body condition. We found that during the first three months of life, changes in antibody concentration were negatively correlated with changes in mass per unit length, skinfold thickness and serum albumin concentration, but only in a sea lion colony exposed to anthropogenic environmental impacts. It has previously been shown that changes in antibody concentration during early Galapagos sea lion development were higher in a colony exposed to anthropogenic environmental impacts than in a control colony. This study allows for the possibility that these relatively large changes in antibody concentration are associated with negative impacts on fitness through an effect on body condition. Our findings suggest that energy availability and the degree of plasticity in immune investment may influence disease risk in natural populations synergistically, through a trade-off between investment in immunity and resistance to starvation. The relative benefits of such investments may change quickly and unpredictably, which allows for the possibility that individuals fine-tune their investment strategies in response to changes in environmental conditions. In addition, our results suggest that anthropogenic environmental impacts may impose subtle energetic costs on individuals, which could contribute to population declines, especially in times of energy shortage.
doi:10.1371/journal.pone.0067132
PMCID: PMC3695956  PMID: 23840603
25.  Habitat dynamics, marine reserve status, and the decline and recovery of coral reef fish communities 
Ecology and Evolution  2014;4(4):337-354.
Severe climatic disturbance events often have major impacts on coral reef communities, generating cycles of decline and recovery, and in some extreme cases, community-level phase shifts from coral-to algal-dominated states. Benthic habitat changes directly affect reef fish communities, with low coral cover usually associated with low fish diversity and abundance. No-take marine reserves (NTRs) are widely advocated for conserving biodiversity and enhancing the sustainability of exploited fish populations. Numerous studies have documented positive ecological and socio-economic benefits of NTRs; however, the ability of NTRs to ameliorate the effects of acute disturbances on coral reefs has seldom been investigated. Here, we test these factors by tracking the dynamics of benthic and fish communities, including the important fishery species, coral trout (Plectropomus spp.), over 8 years in both NTRs and fished areas in the Keppel Island group, Great Barrier Reef, Australia. Two major disturbances impacted the reefs during the monitoring period, a coral bleaching event in 2006 and a freshwater flood plume in 2011. Both disturbances generated significant declines in coral cover and habitat complexity, with subsequent declines in fish abundance and diversity, and pronounced shifts in fish assemblage structure. Coral trout density also declined in response to the loss of live coral, however, the approximately 2:1 density ratio between NTRs and fished zones was maintained over time. The only post-disturbance refuges for coral trout spawning stocks were within the NTRs that escaped the worst effects of the disturbances. Although NTRs had little discernible effect on the temporal dynamics of benthic or fish communities, it was evident that the post-disturbance refuges for coral trout spawning stocks within some NTRs may be critically important to regional-scale population persistence and recovery.
doi:10.1002/ece3.934
PMCID: PMC3936382  PMID: 24634720
Coral reef community dynamics; disturbance; Great Barrier Reef; Marine reserves; Plectropomus spp

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