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On the use of microbiome science for captive breeding management practices in species conservation

Blog post by Pauline van Leeuwen and Jasmine Veitch. Read the full paper here. Featured image of Peromyscus sp. by H. Wilson.

A tiny white-footed mouse covertly scours the woodland forest, looking for a tasty snack. As she makes her way through the forest, the tall maple hardwood stands of the Rouge Valley (Greater Toronto Area) stretch far above her towards the open sky. The moonlight peers through the branches, reflecting off of this small creature’s white coat that extends from the mouse’s bottom lip, across her belly, towards petite foot pads. Huge black eyes blink out from her furry face, her keen sense of hearing and smell on high alert as she surveys her landscape. These features make her remarkably efficient as a nocturnal animal. However, as she continues her journey across the forest floor she is not alone.

Invisible to the naked eye, billions of microbes are moving throughout the forest as well. Some of these microbes are simply spectators to the agile mouse, while others are tiny hitchhikers along for the ride. And what a small world! Viruses, protozoa, fungi, archea, bacteria, all forming communities within an animal, called the microbiota. However, with all these passengers, what can we consider an animal? Is it only the host, or all its microbes as well? With advances in microbiome science, old theoretical questions have been brought back to light from another perspective.

In fact, just as large-scale ecosystems provide services to humankind, the microbiota contribute many vital services for its host. These services, or functions, are beneficial for the host and can be essential for survival (McKenney et al., 2018). In the case of the gut microbiota, it plays a substantial role in breaking down food so the host’s body can absorb and digest it. However, that’s not the only role these microbes play – they also support the body’s resistance towards invasive pathogens through direct competition and modulation of the immune system.

Peromyscus sp. by N. Hrynko

So animals are composed of both animal and microbial cells – but where do these microbes come from? We know that there are two types of microbial transmission. The first one is vertical, where a mother passes on her microbiota to her offspring, mainly during vaginal childbirth for mammals. The second type of transmission is horizontal, where microbes can be acquired throughout an individual’s life; such as from the external environment, social interactions, and diet, to name a few.

We used to think that all microbes were equally distributed across the globe but endemicity and biogeography can influence their dispersal. Some microbes are unique to specific body systems and hosts. Like Darwin’s finches in the Galápagos Islands, each host can represent an island with specific finches (or in this case microbes). Local extinctions of microbes can lead to modification of the services they provide for the host, which can have implications for a host’s survival. A good example is humans. Research on the gut microbiome in humans has already given us a sense that the transition from hunter‐gatherer and nomad societies to farming, sedentary, and then urban lifestyles has altered which microbes hang out in our gut. Especially in Western diets, the lack of fibrous foods and increased consumption of processed foods has resulted in reduction of gut bacteria diversity. Loss of these microbes has been implicated in diseases linked to impaired immune responses (asthma, allergies) and metabolic disorders (obesity, type 2 diabetes; Blaser & Falkow, 2009).

However, this phenomenon also applies to other animals and it can become critical when we consider those on the brink of extinction. Many endangered species are under our care and depend on human intervention for their survival. One tool that we possess to help these vulnerable animal populations is captive breeding programs. Offspring are raised in facilities and then released into the wild to prevent populations from collapsing in their natural habitats. Keeping animals in captivity can be somewhat similar to converting to a human westernized lifestyle, but on a much smaller time scale. Since microbes can be acquired through their external environment, captivity can change microbial communities of a host through standardized diets, reduction in natural and seasonal habitat features, and veterinary care.

Research to date shows that the transition from captivity to the wild leads to changes in the microbiome. Captive animals tend to have less diverse microbes and lower abundance, but not in all cases. If animals with distinct food strategies or gut physiology react differently to captivity, it is important to look at these microbiological processes from a wide variety of animals.

Simulating a captive breeding with white-footed mice by P. van Leeuwen

In our study, we investigated how the microbiome of a generalist and omnivorous rodent, the white-footed mouse, varies according to diet change in captivity and upon relocation to its natural habitat. The goal was to determine if a captive version of a wild diet, with non-processed foods, would foster higher gut microbial diversity compared to dry standardized pellets, once the mice where relocated in their natural habitat. Thus, this experiment simulated the effects of a captive breeding program on the animal’s microbes. We discovered that captive animals under the wild non-processed diet had more bacteria in common with their wild counterparts. Moreover, these bacteria might be beneficial for the mice in terms of food degradation and assimilation.

These results are encouraging and show that management practices in captive breeding programs can be modified to limit the impacts of captivity on an animal’s microbiome and potentially its survival back into the wild. However, questions remain on the actual survival and reproductive success of these relocated mice. More work is needed to look at the specific function of each microbe to its host and to monitor relocated animals in the wild to investigate if changes in management practices have long-term effects. Moreover, similar research into different species with other feeding strategies is highly encouraged. For example, our future work will investigate how herbivorous rodents might experience different changes in their microbiome, like the endangered Vancouver Island Marmot. Thinking back to the tiny white-footed mouse cruising about the woodland forest, one might think twice about what defines the boundaries of an individual. Does she alone make up an animal, or do all her invisible passengers make her what she is?

Back to wild by Pauline van Leeuwen

Blaser, M. J., & Falkow, S. (2009). What are the consequences of the disappearing human microbiota? Nature Reviews Microbiology, 7(12), 887–894. doi: 10.1038/nrmicro2245

McKenney, E. A., Koelle, K., Dunn, R. R., & Yoder, A. D. (2018). The ecosystem services of animal microbiomes. Molecular Ecology, 27(February), 2164–2172. doi: 10.1111/mec.14532

Competition from ants may drive spatial patterns of songbirds in the Eastern Himalaya

Blog written by Jordan Greer. Read the full article here

The foothills of the Eastern Himalaya are a warm, lush ecosystem with trees that reach over 20 meters in height, and a network of branches woven throughout the canopy. At 1500 meters up the mountain, the landscape transforms into cool cloud forest, with cascades of falling moss and an almost ever-present mist. And despite the immense diversity of plants and animals in the cloud forest, ants are almost non-existent.

Ants are found throughout the world, even in harsh environments like the Arctic Circle. Surprisingly, however, most ant species are unable to establish in the mid elevations of the Eastern Himalaya. Some theories suggest that the consistent cold and wet climate of cloud forests prevent ants from establishing their colonies. In contrast, within the foothills ants are in abundance. The dominant ant species at low elevation is the weaver ant (Oecophylla smaragdina)– an insectivorous species that “weaves” leaves together to create nests in tree branches. Highly aggressive, weaver ants guard the trees in which they dwell, and forage for food both arboreally and on the forest floor.  As these common predators are not present above low-elevation, researchers sought to understand how their presence (or lack of it) may impact the surrounding ecological community.

Songbirds are present at both low and mid-elevations, though within the cloud forests the number of species is roughly double. Guided by Dr. Trevor Price, an expert on Himalayan bird biodiversity and Dr. Corrie Moreau, one of the world’s leading ant experts, first author Supriya wished to investigate whether there could be a link between the burst of songbird species and the lack of weaver ants within the cloud forest region. If songbirds and weaver ants foraged for the same insects, the absence of weaver ants could potentially open niche space for more species of insectivorous songbirds to occupy. This could also explain why in the foothills, where weaver ants are common, there are significantly less species of songbirds—by ants acting as resource competitors, they may influence spatial patterns of songbird diversity.

The fossil record could lend support to this idea. Weaver ant species used to be found globally, including Europe. Interestingly, around the same time weaver ants disappeared from the European fossil record, scientists recorded the earliest songbird fossil in Germany. Though speculative, if both animals occupied the same niche, this could act as an early example of how weaver ant presence could influence the spatial patterns and even diversification of songbird species.

Weaver ants carrying insects into their nest in Chapramari Wildlife Sanctuary, India. (Photo: K. Supriya)

To test whether weaver ants could act as a strong resource competitor to songbirds in the Eastern Himalaya, Supriya first needed to establish that both seek out the same food sources. The researchers extracted animal DNA from songbird fecal matter at both low and mid elevation habitat, and compared that to DNA extracted from weaver ant food removed from their colony. The results demonstrated a significant overlap in the diets of weaver ant and songbirds at both elevations— each with a strong appetite for Coleoptera (beetles) and Lepidoptera (butterflies and moths) in particular.

But even though their diets overlap, that doesn’t necessarily mean weaver ants are so voracious in appetite that they exclude birds from occupying habitats by limiting food. To better address this, Supriya asked whether weaver ants significantly depleted the number of arthropods from the trees in which they lived. In the forests near the lowland village of Panijhora, where much of the field research was carried out, she and her field team took on the grueling task of pairing equally sized trees of the same species with and without weaver ant nests. Then they assessed both the insect abundance and the amount of leaf damage present. They found that the abundance of Lepidoptera and Coleoptera was nearly twice as high in trees without weaver ants.

To make sure this finding wasn’t just the result of ant preference for trees with less insects, they followed up with an ant exclusion experiment. Here, the researchers removed all weaver ant nests from several trees and applied a band of TanglefootTM around the trunk to prevent ants from recolonizing. Measures of arthropod abundance were taken before and one month after weaver ant removal. This allowed investigators to tease out if non-ant arthropods could “bounce back” to greater abundance once ants were removed. On average, after one-month trees with ants removed showed 3 times increase in their insect abundance.

Supriya and her 2016 field team (Amir Chhetri, Jobin Varughese, Priyanka Das, Vinod Sankar) sampling arthropods at a tree (Photo: Corrie Moreau)

Taken together, these results suggest that the absence of weaver ants has a positive impact on arthropod abundance. As such, the absence of ants at mid-elevation may contribute to the high non-ant arthropod density within the cloud forest region. In addition, diet overlap analysis shows birds and ants likely compete for arthropod prey at low elevations in the Eastern Himalaya. The lack of competition between ants and songbirds at mid elevation could be one potential driver for the witnessed increase in insectivorous songbird diversity.

A major takeaway from this study is that it is limiting to only look at competition between two closely related species, as is often done. We must also consider the broader communities and guilds in which species take part—these relationships can be as important or more to ecosystem structure. Further, as community ecology research progresses, we need to better address communities that exist across or over regional or environmental climatic gradients, especially in the face of climate change. Could climate change reshape the weaver ants’ distribution to move into cloud forest? And if so, would they displace the resident songbird species? Many questions are left to be answered, but this study acts as an initial step towards tackling questions about community structure within the Himalayas.

Understanding Phylogeographic Histories in an Understudied Region: Historical DNA Coming to the Rescue

Blog written by Haw Chuan Lim. Featured image by Paul van Els. Read the full paper here.

Questions such as why tropical regions are so rich in biological diversity, and how historical and ecological factors shaped the origin and distribution of tropical species have intrigued scientists for generations. Thankfully, exciting improvements in molecular genetics and analytical tools over the last few decades have allowed us to progressively peel back the layers. For example, we now the know the roles large Amazonian rivers and the Andes play in terms of initiating and maintaining species divergence in South America (Naka & Brumfield, 2018).

Image by Paul van Els

Interest in the biogeography and evolutionary history of Southeast Asian plants and animals dates back to Alfred Russel Wallace and earlier. Although researchers have made great strides, especially in the last decade or so (Sheldon, Lim, & Moyle, 2015), it remains a challenge to conduct phylogeographic studies in Southeast Asia. Many areas in Southeast Asia, which is made up of biogeographic subregions such as Indochina, Sundaland and the Philippines, have not been systematically sampled because of logistic and administrative challenges. Further, the region is “feature-packed” when it comes to the diversity of biogeographic processes. In a relatively small area, Southeast Asia contains everything from oceanic archipelagos to continental areas dissected by rivers, mountain ranges and diverse habitat types. Thus, dense sampling is required to produce comprehensive understanding of the historical and geographic drivers of population divergence and speciation.

Grey-throated babbler by Dibyedu Ash, CC3.0

Because of these challenges, past studies have largely taken a piecemeal approach to phylogeographic studies. For example, work in Borneo showed that drier habitats that appeared during past glacial maxima likely caused lowland rainforest species to split into eastern and western forms (Lim et al., 2017). Some studies have shown that the Isthmus of Kra, the narrow land bridge in southern Thailand that connects Sundaland and Indochina also separates sister species or closely related populations (Manawatthana, Laosinchai, Onparn, Brockelman, & Round, 2017).

Black-headed Bubul, by Doug Janson CC3.0

In this study, we used techniques that allow us to sequence thousands of genetic markers using DNA extracted from old (from late 1800’s onwards) museum study skins to investigate phylogeography of five species of rainforest-associated passerine birds that co-occur across much of Indochina and Sundaland. While technically challenging, this approach let us achieve comprehensive and relatively even geographic sampling for each of the five species. The massive amount of genetic data generated enable high-resolution studies of population structure and historical demographic processes, thus providing insights that were previously unavailable.

Large Niltava by Ajit Hota, CC4.0

We discovered that the phylogeographic patterns of the study species largely agree with their ecological characteristics. The Black-headed Bulbul, a frugivore/insectivore species that often uses forest edges, shows little population genetic structure across the entire Sundaland and parts of western Indochina. In contrast, the Little Spiderhunter and Asian Fairy-Bluebird possess highly distinct populations in peripheral Sunda islands (Java and/or Palawan) and India. This is probably due to their intermediate dispersal abilities, which allowed them to colonize new areas, and then remain largely isolated subsequently. Such dispersal events could occur during periods of low global sea-level, which exposed land bridges. A north-south population break across the Isthmus of Kra is shared only by the two species (Gray-throated Babbler and Large Niltava) that live in hill/submontane habitats. This suggests that the low elevation of the Isthmus of Kra had contributed to population splitting or the maintenance of population separation in the two species.

Little Spiderhunter by Lip Yee Kap, CC2.0

Interestingly, the Black-headed Bulbul and Gray-throated Babbler, two species with different ecological characteristics, show an east-west break in Indochina. This break is associated with the central mountain (Tennasserim) range of Indochina or the dry Irrawaddy plains of central Myanmar. Without the use of DNA from old museum skins, the discovery of genetic breaks in this region will be very difficult because it has rarely been visited by museum scientists in recent years. In each of the five species, the deepest split dates back to 1-1.5 million years ago. This coincidence in timing suggests that region-wide environmental upheavals –likely those associated with glacial cycles – played important roles in splitting populations and structuring genetic diversity.

Asian Fairy-Bluebird by Tony Castro, CC4.0

With the accelerating loss of forest habitats across Southeast Asia, it is imperative that we improve our understanding of what makes up significant evolutionary units within species, and what historical, environmental and geographic factors caused these units to form and persist. Advances in phylogeographic studies in Southeast Asia, a biologically rich region composed of multiple biodiversity hotspots, will depend on broad geographic sampling and the use of increasingly sophisticated molecular genetics and analytical techniques.

Picture by Haw Chuan Lim

Lim, H. C., Gawin, D. F., Shakya, S. B., Harvey, M. G., Rahman, M. A., & Sheldon, F. H. (2017). Sundaland’s east–west rain forest population structure: variable manifestations in four polytypic bird species examined using RAD-Seq and plumage analyses. Journal of Biogeography, 44(10), 2259-2271. doi:10.1111/jbi.13031

Manawatthana, S., Laosinchai, P., Onparn, N., Brockelman, W. Y., & Round, P. D. (2017). Phylogeography of bulbuls in the genus Iole (Aves: Pycnonotidae). Biological Journal of the Linnean Society, 120(4), 931-944.

Naka, L. N., & Brumfield, R. T. (2018). The dual role of Amazonian rivers in the generation and maintenance of avian diversity. Science Advances, 4(8), eaar8575. doi:10.1126/sciadv.aar8575

Sheldon, F., Lim, H. C., & Moyle, R. (2015). Return to the Malay Archipelago: the biogeography of Sundaic rainforest birds. Journal of Ornithology, 156 (Supplemental 1), 91-113.

Family life on a cadaver

Blog written by Eva Keppner & Sandra Steiger. Read the full paper here.

Parental care – investing energy and time to raise and protect offspring – can be observed in many species spread all over the animal kingdom. Drivers of the evolution of parental care seem to be, among others, a harsh environment, a structured habitat or ephemeral resources. Interestingly, it is often only the female parent who does most of the work and the males wander off in search for new mating partners. However, sometimes male and female together form a family unit for a certain amount of time and raise their offspring in a joint endeavor.

It is not quite clear what exactly leads to the participation of the male. Much of what we know about the mechanisms of biparental care came and still comes from research on birds, where males and females often share the burden of raising their offspring. Some years ago (although thoroughly described already in 1933), another organism moved into the spotlight of the study of parental care: the burying beetle. Beetles of the genus Nicrophorus show an elaborate set of parental care behaviors, both males and females are capable of preparing an adequate nursing environment, feeding and protecting their larvae, as a pair or a single parent. The nursing environment, a small vertebrate carcass, e.g. a mouse or a small bird, also conveniently serves as the sole food source for the whole family during reproduction. This detail of their biology played the main role in our study. We wanted to disentangle the benefits of two caring parents from the downsides of two parents eating from the family’s dinner table instead of only one.

A male and a female burying beetle working together during post-hatching parental care. Featured image above shows a male burying beetle sitting on a mouse cadaver (Both images by Heiko Bellmann)

Parental behaviors in burying beetles comprise pre- and post-hatching activities. During pre-hatching care, the parents bury and prepare the carcass so it is suitable for their soon-to-arrive larvae. We first compared parent pairs and single females during this approximately three-day task. Almost all of 163 experimental beetles gained weight during this time and the carcasses, which were of very similar weight at the beginning, lost more weight when prepared by two beetles instead of one.  Consequently, most of the beetles have eaten from the carcass and two beetles eat more than only one. Hence, pairs have less food available in the post-hatching phase, where larvae are fed with regurgitated carrion and also self-feed from the cadaver. Quite obvious one might think. But this is where it gets interesting (for us biologists at least…). Most studies that compared the efficiency of bi- vs uniparental care in burying beetles used the same set up: a single female or a pair of beetles receives a carcass of the same size and offspring fitness is used as a measure of brood success. Within this study design, offspring fitness never differed between uni- and biparental condition. Additionally, it is known that carcass size influences brood success in burying beetles. So why do carcasses which are no longer of similar size at the time of larval hatching, due to the amount eaten by one or two parents, not lead to a noticeable difference in offspring fitness between uni- and biparental conditions, like bigger or more larvae?

In other words, why does our single female with a bigger carcass at the time of larval hatching not raise more or heavier larvae than a pair of beetles with a smaller carcass? Probably because she is missing the help of a second caring parent, the male beetle. To find out if this assumption is true, we performed another experiment. Again, we provided single female and male/female pairs with carcasses of similar sizes. However, this time we switched the carcasses after preparation by the beetles shortly before larval hatching. Now the beetle pairs had bigger carcasses than the single females (only slightly bigger – we’re talking of differences in the range of milligrams). Pairs reared heavier broods than single females. Therefore, we were able to find some support for our initial assumption that two beetles are better in caring for their offspring but this effect is often masked because a male parent also eats from the resource, which leaves the rest of the family with less food. We only found this effect for small carcass sizes when food is limited.

We tried to also align our findings within the evolution of biparental brood care in burying beetles and started some speculations. As female N. vespilloides as well as females of other species in this genus are perfectly capable of preparing the carcass and rearing the offspring alone, why did biparental care evolve in the first place? One certain benefit of a male beetle is brood protection against unwanted intruders (mainly other burying beetles). This might have been the first step. Of course, a male sitting guard at the brood chamber could hardly resist the smell of a food source – and also started eating from the carrion, leading to an imbalance again, as everything he eats is no longer available for his progeny. Males, who were also able to provide more than just safety by also feeding the offspring might have been better fathers by rearing heavier larvae which will eventually hatch into bigger adult beetles. Which led to the state of care we can now observe in burying beetles.

With our simple experimental set-up, we were able to gain a little insight into the mechanisms of family life. However, this field of research with its intertwined relations and behaviours between family members is incredibly exciting and still offers a lot to find out. 

Wildflower Power: wildflower plantings benefit blue orchard bee reproduction in commercial orchards

Blog written by Natalie Boyle. Read the full paper here.

Insect-mediated pollination provides an essential ecosystem service to wild and managed landscapes, and ensures the production of food, fuel and fiber that is vital for human survival.  Today, honey bee health is challenged by many overlapping stressors that have resulted in sustained annual losses of one-third of all honey bee colonies in the United States.  At the same time, recent and alarming declines in insect biodiversity worldwide have highlighted the need to turn to agricultural practices that better support native, beneficial insect populations—including bees, predators of insect pests and natural enemies.

Wild or alternative bee populations frequently play an important but underappreciated role in modern crop pollination.  However, recent studies have illustrated the significance of non-honey bees in the pollination of various regions and cropping systems, including California almond groves, Pennsylvania pumpkin patches and New York apple orchards.  Recognizing the value and contribution of ‘other bees’ to agriculture is essential, as migratory beekeeping operations have struggled to meet the pollination demands of a fast-growing agricultural sector.  While the European honey bee is indisputably the most well-studied bee, it’s important to remember that they are just one of over 20,000 described bee species worldwide.  The study and promotion of alternative pollinators has only just recently come into the public spotlight.

Perhaps no other industry is impacted so heavily by current honey bee colony losses as the California almond industry, which relies entirely upon contracted hive rentals to ensure profitable yields. Responsible for 80% of global almond production, and with over 1 million acres of nut-bearing orchards, the California almond industry requires over 1.9 million (ca. 73%) of the nation’s honey bee colonies to meet pollination demands.  By making some simple adjustments to the management and land use of bare areas near almond orchards, we propose that some of this pollination burden can be offset by the supplementation of alternative native pollinators in Western tree fruit and nut orchards—and in California almond orchards in particular.

A BOB visits a Phacela ciliata blossom in a wildflower planting

The blue orchard bee, or ‘BOB’, is a native, solitary bee species whose range expands across the United States.  Unlike honey bees, BOBs do not live as colonies or make honey.  Instead, individual females nest in abandoned wooden beetle burrows, or in hollow reeds and stems – however, for management purposes, they will nest readily and gregariously in artificial nesting tunnels made of cardboard tubes or drilled holes in wood blocks. Each BOB female builds her nest as a serial set of five to ten brood cells, each provisioned with a mass of pollen and nectar onto which a single egg is laid. The end of each cell is sealed with a sculpted mud partition, whereby female BOBs earn their alternative title as ‘mason bees.’

BOBs are ideal pollinators of commercial orchards because they prefer foraging on rosaceous crops, and collect pollen dry in specialized hairs on their bellies known as ‘scopae.’ This mode of pollen storage promotes higher rates of pollen delivery to blossoms when compared to honey bees, who tightly pack away pollen in specialized baskets on their hind legs (known as corbiculae).  BOBs forage in cooler weather than honey bees and are active as adults for just 4 – 6 weeks of the year:  This active period can be manipulated through established temperature-controlled incubation to occur at any time from early February to late May, which provides flexibility in management.  Previous studies have already demonstrated the economic benefit of BOB pollination in commercial almond and cherry orchards. However, high (~60 – 70%) dispersal of managed BOB populations has to-date prevented widescale adoption of the practice in most agricultural landscapes.  Without sustainable rates of annual in-orchard BOB retention and reproduction, their implementation as alternative pollinators is cost-prohibitive, as a grower would be required to replenish their supply annually.

Five completed BOB nests (‘tunnels’) collected from experimental almond orchards.  Sex and progeny outcome are determined from X-radiography after progeny have developed to the adult stage

Currently, BOBs are sold from limited stores and at high financial and ecological costs.  The industry is supported by cleaning, sorting, storing and distributing bees captured from wild habitats, which is environmentally and economically untenable.  Identifying practices to maximize in-orchard reproduction of managed BOB populations is the best strategy to protect the stability of wild BOB populations while also reducing annual pollination costs to orchard managers.  The objective of our study was to determine whether the installation and maintenance of native wildflower plantings could support local populations of managed BOBs in commercial almond orchards.

Using established best management practices, we introduced managed BOB populations to a total of 72 acres of commercial almonds to evaluate their reproductive success in relation to three nearby 1-acre wildflower plantings.  The wildflower plantings bloomed concurrently with and beyond almond bloom, which enhanced the diversity of pollen and nectar available to foraging bees and extended their foraging period (almonds generally bloom for just two to three weeks – which effectively halves the typical foraging period for female BOBs).  We evaluated how proximity to wildflower plantings influenced BOB reproduction and progeny outcomes over the season throughout 2015 and 2016.

We found tremendous value in the introduction of wildflower plantings to almond orchards. In 2016, 80% of the females released were recaptured as progeny for use in the next year.  Wildflower pollen was frequently and regularly incorporated into BOB provision masses, even at distances 800 m away from the wildflower plantings.  Additionally, the most progeny were recovered from areas closest to the plantings.  We also saw that landscape context was important in supporting BOB populations, as higher reproduction was consistently observed along orchard edges versus within orchard interiors.  Further, our wildflower plantings required a relatively small commitment of land and labor compared to neighboring cropland.  This study shows that installing wildflower habitat is a promising strategy for California orchard managers wishing to incorporate BOBs sustainably into their own pollination regimes. 

Our work shows the benefit of planting flowers near crops with limited bloom timing. There is growing interest in the adoption of alternative pollination, as is evidenced by the success of the Bee Better Certified label. A collaborative creation of the Xerces Society and Oregon Tilth, this label rewards agricultural producers for the establishment of floral habitat alongside agricultural crops to benefit wild bee and beneficial insect populations.

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