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A new approach for ecosystem-scale manipulations of bird abundance and species richness

Blog written by Chelsea L. Wood. Read the full paper here.

For generations, ecologists have relied on manipulative experiments to explore the dynamics of ecological communities. Some of the most influential studies in the ecology canon are experimental manipulations – think Bob Paine’s experimental exclusion of the keystone predator Pisaster ochraeceous, Stephen Carpenter’s whole-lake manipulation of nutrients, Dan Simberloff and EO Wilson’s island biogeography experiments in the Florida Keys, or Gene Likens’ forest-clearance experiments at Hubbard Brook. Correlational and comparative studies have their place for detecting and exploring the generality of patterns, but experimental manipulations are needed to understand the causal relationships that underlie ecological patterns.

But despite the value of manipulative experiments, they can be exceedingly difficult to execute, particularly when the focal community contains large-bodied, vagile species. For example, several studies point to the ecological importance of birds as predators, nutrient importers, hosts, seed dispersers, pollinators, and scavengers. But progress in understanding the ecological role of birds at the ecosystem level has been hampered by the difficulty of performing experimental manipulations of bird abundance across large spatial extents.

Our paper, recently published in Ecology and Evolution, presents a new method for experimentally increasing the abundance and richness of birds at the scale of entire aquatic ecosystems, with minimal cost, risk to wildlife, and need for maintenance. This approach involves the use of attractants that encourage birds to use a particular site, instead of deterrents that discourage birds from using that site or physically preventing their access to the site (approaches whose efficacy often attenuates over time). Our approach was effective at increasing the abundance and species richness of water‐associated birds at central California ponds.

Figure 1. Map of study sites in the East Bay region of central California. Eight experimental ponds were located in Joseph D. Grant County Park (circles) and eight were located on San Felipe Ranch (triangles). Of these, eight were randomly assigned to the bird attractant treatment (blue) and eight were randomly assigned to the control treatment (red)

We worked at 16 small ponds located on two adjoining properties in the East Bay area of central California (Figure 1). To attract birds to attractant‐treatment sites, we added perching habitat, nesting habitat, two mallard duck decoys (one male, one female), and one floating platform to each pond (Figure 2). We then assessed bird abundance by monitoring ponds with trail cameras. We compared the change in bird species richness and abundance from before the manipulation (i.e., 2014) to two years after manipulation (i.e., 2017) in control versus attractant treatments (a before–after–control–impact or BACI design).

Figure 2. Attractant manipulations installed at Glorious Pond, Joseph D. Grant County Park. bb = bird nesting boxes, fp = floating platforms, yellow arrows indicate added perching habitat

We found that our bird-attractant treatments augmented both bird species diversity and bird abundance. Bird species richness declined over time in both treatments, probably due to the effects of a prolonged drought that affected California during the time period of our experiment, but the decline in bird richness was less pronounced in the attractant compared to control treatments. Total bird abundance (across all species) increased in the attractant treatment while it declined in the control treatment. The bird species in which the attractant treatment had the most positive influence on abundance were American Robins, Black Phoebes, California Quail, Western Kingbirds, unidentified passerines, raptors, and waterbirds; together, these taxa accounted for 83% of total bird detections.

Our results suggest that simple, inexpensive modifications to existing pond habitat can produce a substantial change in bird abundance and richness – providing a way forward for field experiments that effectively quantify the ecological role of birds. It is especially notable that the manipulations were effective two years after their implementation; this allows for experiments with long temporal durations, a key feature for assessing ecological processes that occur on long time scales.

The manipulations we implemented were inexpensive, easily maintained, and unobtrusive. We estimate that our attractant treatments cost approximately US$103 per pond ($60 for wood duck box, $25 for generic bird box, $2 for fence posts to mount bird boxes, $6 for duck decoys, $10 for materials to construct floating platform), and required fewer than two person‐hours to install. In addition to their low cost, our manipulations were durable and easily maintained: despite the presence of large mammals (e.g., deer, pigs, coyote, cows) that might trample or otherwise compromise attractants, we observed no negative wildlife interactions. Manipulations required very minimal maintenance; we checked on ponds once per year and spent ~15 person‐minutes per pond per year re‐positioning floating platforms or duck decoys, supplementing shoreline perching habitat, or (for only one pond over the two‐year experiment) re‐mounting a fallen bird box. Importantly, the manipulations were unobtrusive and inconspicuous. This low visibility minimizes the chance that the treatments will be noticed by human visitors, reducing the likelihood of vandalism, theft, and objections by neighbors, park users, landowners, or land managers concerned about the aesthetic value of ponds. In fact, one of the land managers we worked with was enthusiastic about these manipulations, which she hoped would contribute to the conservation value of wetlands under her stewardship. The low cost, ease of maintenance, inconspicuousness, and conservation benefits of our approach allowed us to maximize the size and number of manipulated ponds, increasing statistical power and biological realism.

There are numerous potential applications of our approach to manipulating bird abundance and richness. We plan to use this method to perform a large‐scale, long‐term bird manipulation experiment in central California ponds. Our aim is to quantify the effect of increases in local bird abundance and richness on the composition of pond communities, and particularly on the transmission of parasites within ponds. Birds play a variety of roles in these pond ecosystems: as dispersers of parasites, predators of hosts, and hosts for vectors and the pathogens they transmit. Manipulative experiments are therefore necessary to disentangle the potential effects of change in bird biodiversity on disease processes and to discover the net effect of bird biodiversity loss on the prevalence of disease in ponds. Our method of bird augmentation might also be useful for scientists working on other questions about the ecological roles of birds, or in other ecosystems. Most bird manipulation experiments to date have investigated the role of birds as predators using bird deterrence, and bird exclusion is a suitable approach for assessing the impacts of bird predation on community composition at small spatial scales. However, because our approach can be deployed across larger spatial scales than traditional caged or netted bird exclosures, it can also be used to investigate processes that occur at large spatial scales: for example, nutrient export/import, seed dispersal, and scavenging/decomposition. Our approach could also be easily adapted to augment birds across large plots in other relatively open ecosystems—for example, grasslands, meadows, open woodlands, tundra, marshes, wetlands, dunes, and beaches.

The vanishing ghost butterfly and a faint hope for their continued existence in urban forests fragments

Blog written by Antonio C. de Andrade & Matthew Adams. Read the full paper here.

There is a large, white butterfly (Morpho epistrophous nikolajewna) that still flies within the Brazilian Atlantic forest; once common, but now vanishing. Unfortunately, we only have a vague idea of what could be driving this species into oblivion.

The Brazilian Atlantic forest was at the front line of the havoc wrought by the early Europeans centuries ago. By fire and axe, as so elegantly and poignantly described by Dean (1995), the forest was converted to a small patchwork of forests that today is mostly immersed in sugarcane fields. Yet forest fragmentation is not the sole culprit for the demise of the ghost butterfly. There are other agents at work, some obvious (e.g. pesticides and logging) and other not so obvious (subtle local microclimate alteration and by-products of agricultural practices). Our paper details a history of loss, but also hope, which was found in an unexpected forest sanctuary surrounded by roads, buildings and all the urban chaos that can stress wildlife.

Sugarcane burning. Photo by Craig Elliot, FreeImages

The deleterious effects of human activities are greatly augmented in cities. The best example, and perhaps the most emblematic, is vehicular pollution. Thus, we were quite amazed to find a thriving population of ghost butterfly in an urban forest fragment, which are often subject to profound additional environmental stresses compared to rural ones.

The side effects of anthropogenic activities can be scary, yet it is difficult to comprehend their magnitude and how exactly they affect the biodiversity. For example, a group of amateur German entomologists and scientists (Hallmann et al. 2017) reported an alarming 76% decline in the biomass of flying insects over a period of 27 years in protected areas. They could not pinpoint the precise driving forces responsible for this decline, although suggesting agricultural intensification (e.g. pesticide use and habitat loss) as a plausible cause.

It was disappointing, but also important, to find out that many suitable areas failed to maintain populations of this butterfly. Why is the ghost butterfly absent from larger and well-preserved rural forests, while occurring in an urban forest fragment? This is puzzling. The most striking difference we found between these fragments is that all rural fragments we surveyed are surrounded by a matrix of sugarcane that is burned before harvesting, and perhaps during the ghost butterfly’s development they could be subjected to higher particulate pollution in rural fragments.

Pre-harvest burning of sugarcane is a widespread practice – the crops are burned in order to facilitate the harvesting process. The resulting smoke contains harmful gases and tiny particles. Insects can be sensitive to changes in air quality due to the direct way the air enters cells inside their body; they breathe via spiracles, valve-like openings on the outside of their exoskeleton. These openings connect to internal tracheal tubes that form a branching network that reach every part of the insect’s body. We think the effects of the pre-harvesting burning might have a negative effect in the ghost butterfly population, and may have previously been neglected.

It is noteworthy that the proportion of silicon dioxide (SiO2) in the sugarcane ashes is quite high (Le Blond et al. 2010) and could act as insecticide on herbivores (Edwards & Schwartz, 1981). The deposition of particulate, with a high amount of silica, on leaves inhibits feeding, which probably occurs via  physical action by wearing down the mandibles due to the abrasiveness of ashes/dust. Ashes could also cause the impairment of the spiracular function leading to respiratory stress (Elizalde 2014).

Dorsal and ventral views of male ghost butterfly. Photo by Andre V. Lucci Freitas.

The wider implications that the pre-harvest burning of sugarcane might have an impact on biodiversity remains speculative, yet plausible. The presence of a population of butterflies in one place, versus absence at several other places, does not provide unequivocal support for the assumed drivers of rarity. Indeed, the full extent of the effect of smoke pollution still needs to be investigated. Unambiguous evidence of the mechanism we suggest would require some experimental manipulation e.g.  transplants of caterpillars/adults to fragments surrounded by pasture, or experimentally smoking caged individuals using sugar cane residue.

We suggest that the long-life cycle of the ghost butterfly makes it especially sensitive to the sugarcane burning pollution. In this sense, it is interesting to highlight that the endangered M. menelaus eberti occurs in one larger rural fragment – Gargau. This species has multiple generations per year (Andre V. Lucci Freitas, personal communication).

Of course, there could be a number of other hypotheses for causal agents of decline, but in these cases, one would need to show change in abundance through time, and the causal agent of decline. Monitoring ghost butterfly population in urban areas, and comparing these to populations in rural forest remnants is essential to provide a foundation for the assessment of suitable habitats and elucidate the key drivers affecting population dynamics of the ghost butterfly within the Brazilian Atlantic forest.

Our paper shows the importance of native urban forest remnants for conservation i.e. unexpected sanctuaries given the pollution found in cities. Whether urban pollution will drive these populations to evolve, or disappear into oblivion, remains unknown. Human activities have a profound effect on biodiversity and our study serves as a warning regarding the many, often subtle, ways that these activities can cause rarity of once common species.

References

Dean, W. (1995) With broadax and firebrand: the destruction of the Brazilian Atlantic forest. University Press of California.

Edwards, J.S. & Schwartz, L.M. (1981) Mount St. Helens ash: a natural insecticide. Canadian Journal of Zoology 59, 714–715.

Elizalde, L. (2014) Volcanism and arthropods: a review. Ecologia Austral 24, 3–16.

Hallmann, C.A. et al. (2017) More than 75% decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, eo185809.

Le Blond, J.S. et al. (2010) Generation of crystalline silica from sugarcane burning. Journal of Environmental Monitoring 12, 1459-70

The role of reef sharks in structuring predatory fish communities after recovery from illegal fishing

Blog written by Mark Meekan & Conrad Speed. Read the full paper here.

Predators structure prey communities both through consumption and by altering the behaviours of their prey. Prey that is wary of a predator is less likely to use a risky habitat and will spend more time being vigilant, which can be costly as it can mean that there is less time for foraging and reproduction. Such influences of predators on prey communities are well documented in terrestrial and some aquatic ecosystems but remain largely unstudied on coral reefs.

Although sharks are the most obvious and ubiquitous large predator in reef environments, research into their effects on fish communities is both limited and controversial. Because sharks can move over large distances and are slow to reproduce, experimental studies that seek to examine the role of sharks as structuring agents by excluding or removing them from reefs are fraught with logistic and ethical difficulties. However, due to fishing, populations of reef sharks in many areas have been in steep decline.

Some researchers have used this situation as a “natural experiment” to compare fish communities of reefs where sharks have been removed to communities on other reefs where populations remain intact. Such studies suggest that sharks may affect the abundance, trophic role and morphology of mesopredatory fishes at lower or equivalent positions in the food chain.

These conclusions are controversial, because fish communities can also differ between reefs due to habitat quality, productivity and the history of natural and anthropogenic disturbances. To avoid these issues, our study used a different approach. Instead of comparing communities between reefs, we looked at how fish communities have changed on the same reef where the enforcement of a no-take Marine Reserve and cessation of illegal fishing has allowed reef shark and fish communities to recover through time. As the reader might imagine, given the current state of the world’s oceans, such opportunities are very rare. 

We worked at Ashmore Reef, a remote atoll located hundreds of kilometers northwest of Australia. The reef is a no-take marine reserve that has had near-fulltime protection of its borders by Australian Customs and Border Force since 2008. Enforcement was essential due to the numbers of vessels fishing illegally in the area, many of which targeted sharks for their fins.

Our earlier work (Speed, Cappo and Meekan 2018) has already shown that shark numbers at Ashmore Reef have recovered at a remarkable rate – up to six times the pace predicted by demographic models. Today, shark abundances on Ashmore are 4.6 times the numbers we recorded before protected status was enforced. But what happened to the rest of the predatory fish community? To find out, we compared data collected by baited remote underwater video stations (BRUVS) in 2004 (prior to enforcement of the reserve), with a more recent BRUVS survey in 2016, which occurred after eight years of strict protection of the reef in 2008. The 2016 survey was conducted as part of the Global FinPrint Project (https://globalfinprint.org/).

The illegal fishing that targeted sharks also caught other large predatory fishes, so it is not surprising that these also recovered once fishing was stopped. In comparison to 2004, large mesopredatory fishes (> 100 cm in length) – species such as the big snappers and large trevallies (jacks) – increased in numbers by a factor of 2.3. The story was similar for medium-sized mesopredators (50 – 100 cm in length) which were mostly coral trout, snappers and emperors. These increased in abundance by a factor of 1.5. However, outcomes were very different for small mesopredators (< 50 cm in length). These species declined in abundance by a factor of 2.5 between 2004 and 2016. Today, abundances and size structures of the shark and fish faunas of Ashmore Reef are comparable to those of other “pristine” reefs in the region nearby, suggesting that fish and shark communities have largely recovered from exploitation.

The changes in abundance of mesopredators at Ashmore Reef we recorded are consistent with theories and observations of how large predators structure trophic pyramids. When large predators are removed, smaller mesopredators become abundant, a phenomenon known as “mesopredator release”. Conversely, when populations of large predators recover, abundances of smaller mesopredators are suppressed. It is difficult to separate the relative contributions of reef sharks and the other large mesopredators to our result. However, it is interesting that we found only a small change over time in the numbers of smaller mesopredators in the near-reef habitats (areas of sand and rubble adjacent to the coral reef) we sampled with BRUVS. In this habitat there was a much smaller increase in shark numbers, but an increase in the abundance of larger mesopredators (by a factor of 2.3) similar to the one that occurred on the reef. This implies that abundances of reef sharks were more influential than large mesopredators in determining changes in numbers of smaller mesopredators.

Why did these changes in numbers of small mesopredators occur? The obvious answer is that predation by larger predators was a key driver, but the story is not likely to be so simple. For example, we found some evidence that certain species of smaller mesopredators moved to different habitats when predation pressure changed. Although total numbers of the spot-cheek emperor (Lethrinus rubrioperculatus) did not vary between surveys, the species occurred in highest numbers in reef habitat in 2004, when there were few sharks and large mesopredators. In 2016, the same species occurred in highest abundances in the near-reef habitat, where there were fewer sharks.

Overall, our results are consistent with earlier studies in NW Australia that used spatial comparisons among reefs with and without sharks to examine the role of these predators in fish communities. These studies also found evidence for mesopredator release in smaller size categories of reef fishes. Although the mechanism(s) underlying the changes we observed in some parts of the fish communities remain to be documented, our study does provide a very positive message for managers and researchers working toward the conservation of coral reef ecosystems. The predatory fish communities of coral reefs, which are invariably the primary targets of exploitation and are so often over-fished in many places around the tropics, can recover at an unexpectedly fast pace. Our study shows that well-enforced marine reserves could play a key role in making this happen.

References

Speed CW, Cappo M, Meekan MG. 2018. Evidence for rapid recovery of shark populations within a coral reef marine protected area. Biological Conservation 220:308-319.

Emerging from the cocoon: Digital butterfly collections shed light on the intricacies of temperature-size responses

Blog written by Rebecca Wilson. Read the full paper here.

On some days, the Natural History Museum (NHM) in London may seem like an over-crowded hall of curiosities, where visitors come only to stare at the big animals, like the dinosaurs or the whale skeleton hanging from the ceiling. But look closely and you’ll find that the smaller and more common specimens housed at the NHM are worth paying attention to. Deep in the cocoon and maze of underground corridors lie millions of specimens, including a wide range of species collected globally, from fossils and dating back millions of years ago to modern specimens collected in recent years. These specimens not only provide us with an insight into the biological world of the recent and distant past but when used to good effect, can help us answer some of nature’s most complicated questions of today.

‘The Cocoon’ in the Darwin Centre at the NHM, houses many laboratories and specimens, which can be viewed by the public. Photo credit: Phil Fenberg

Insects are one of the most common and diverse groups of animals on Earth. The NHM is home to millions of insect specimens from across the world, but the majority of these specimens are hidden away in drawers away from the public eye…until recently that is. In the past few years many of these specimens and their meta-data (location and date of collection) have been photographed and turned into digital online collections. The iCollections, for example, includes all British butterflies and moths held in the museum. Thus, these hundreds of thousands of specimens are now globally available for researchers, which would not have been previously possible without physically visiting the museum and handling their delicate bodies.

In our paper, we sought to evaluate the research utility of the iCollections to help answer a recent question nagging ecologists: Will the body sizes of animals get smaller in response to climate warming? Reduction in body size has been suggested to be one the “universal” ecological responses to climate change, but recent studies suggest that insects may have more complex responses – which may be due to their complicated life cycles. We used images from the iCollections to analyse how adult body size changes with temperature for three British butterfly species. Our study species were the Adonis Blue (which has two generations per year), the Chalk Hill Blue (one generation per year) and the Silver-studded Blue (one generation per year). As the names suggest, these butterflies can easily be spotted due to the distinctive blue colour of the males’ wings (or the orange spots on the edges of the brown female wings). The Adonis Blue can be seen on south facing chalk hills from May to June (generation one) and August to September (generation two) alongside the Chalk Hill Blue from July to September, whereas the Silver-studded Blue can be found on a variety of habitat types, most commonly on heathlands, in July and August.

Adonis Blue (male) photographed on the chalk hills at Beachy Head (Eastbourne) in early June

We measured the forewing lengths of each specimen from the images. Average forewing lengths were analysed alongside mean monthly temperatures (from the MET office), coinciding with the caterpillar stages of each species. Furthermore, males and females were analysed separately and for the Adonis Blue, generation one and two were also analysed separately to determine if the sexes and/or generations respond differently to temperature.

Adonis Blue specimen from the iCollections. The imbedded scale bar (bottom) was used to set the scale in Image J, then lines were drawn to measure forewing lengths (white lines).

For the males of each species, we found that adult size increases with temperature only when temperatures are high during late stages of caterpillar growth but adults decrease in size with increasing temperature during early stages of caterpillar growth. Females, on the other hand, showed varying responses between the species, with some following the same pattern as males and some showing no response at all. Additionally, the second generation of Adonis Blue also showed no response to temperature for males or females.

Responses of early and late stage caterpillars to temperature for males and females of each species (and each generation for Adonis Blue).

Our results highlight both the importance of analysing males and females separately, and the usefulness of museum collections for research into biological responses to climate change. The variations in responses between species are likely due to the specific ecological and environmental conditions they grow in, while the differences in responses between males and females are potentially due to whether earlier emergence is more important than growing for longer (and to a larger size) for individuals of each sex. We also show that responses can differ between caterpillar stages, and therefore, how future increasing temperatures will affect adult size will depend upon which months are warmer than average.

With improvements in technology coming thick and fast, the avenues for collections-based research are ever expanding. Advances in machine learning, for example, could mean that time sapping tasks such as exhaustive manual measurements of physical or digital specimens will become a thing of the past. In the near future, computers will be able to measure these specimens for us in a fraction of the time, and therefore, we will be able to analyse a wider range of specimens to determine if the patterns we found for our three species are consistent across other butterfly species. Our study represents just one example of how digital museum collections can be a useful tool for climate change research.

Whether pinned, encased in a slide, sitting in a jar or cardboard box, the millions upon millions of natural history specimens housed in the back rooms and basements of natural history museums across the globe are now ready to pose for their picture, and with technology improving at an ever advancing rate, the possibilities for future research are endless.

Avoiding roads: reptiles take paths less travelled

Blog written by James Paterson, Julia Riley, and Christina Davy. Read the full paper here.

There are currently more than 21 million kilometers of roads across the world. As the human population grows, that number is set to double in the next 30 years. Vehicle strikes are responsible for a large amount of wildlife death when animals cross roads. But, do roads also have less obvious impacts on wildlife? If crossing a road is risky, it may limit access to preferred habitats. Many animals avoid roads, like birds, caribou, and many reptiles, but no study has previously looked at how avoiding roads may affect a reptile’s energy costs or examined if animals avoid roads across multiple study sites.

We tracked turtles and snakes using radio-telemetry. Photo: Julia Riley

We studied two endangered species that often live near roads. Blanding’s turtles (Emydoidea blandingii) are medium-sized turtles that live in wetlands around the Great Lakes in North America. Eastern massasaugas (Sistrurus catenatus) are small, semi-aquatic rattlesnakes that live in wetlands, prairies, and alvars. We hypothesized that roads may change the behaviour of these reptiles, and that avoiding roads may be energetically costly. We predicted reptiles would avoid roads and reptiles living near roads would spend more energy moving because they have to travel further to reach their preferred habitats. To test these predictions, we used individual tracking data on 286 turtles and 49 snakes from 18 sites in eastern North America.

We found that turtles and rattlesnakes avoided crossing roads, but they didn’t avoid habitat near roads. Many turtles and snakes in our study still crossed roads, but they did so at a lower rate than we expected based on simulated paths.


Eastern massasaugas (Sistrurus catenatus) avoided crossing roads but did not avoid habitat near roads. Photo: Julia Riley

Rattlesnakes near roads did not move more than rattlesnakes living in areas without roads. In contrast, turtles living near roads spent more energy moving than turtles that didn’t live near roads. But, is this difference relevant to fitness? The extra energy spent by turtles near roads was less than the energy required to produce one egg. To put that in perspective, Blanding’s turtles lay between 8 and 25 eggs each year. Although living near roads resulted in higher energy costs, this difference is unlikely to significantly reduce the reproductive output or survival of turtles.


Blanding’s turtles (Emydoidea blandingii; left) with roads in their home ranges moved farther per day and spent more energy moving than turtles without roads in their home ranges. Eastern massasaugas (Sistrurus catenatus; right) with roads in their home range did not move significantly farther per day than snakes without roads in their home range. Photos and Figure: James Paterson

Our results suggest that reptiles change their behaviour in response to roads, but mortality from vehicle strikes remains the biggest known impact of roads on these populations. Future research should continue to explore ways to reduce wildlife mortality on roads, such as exclusion fencing and conservation-focused road planning.

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