It’s a wasp…It’s a leaf…It’s a moth: Moth mimicry

The tropics are recognized as biodiversity hotspots (Gaston 2000) and this is particularly apparent in Lepidoptera, the order of insects that includes moths and butterflies. The warm temperatures of the tropics and constant food supply allow these insects to stay in one area and not have to migrate. The families have diversified so much that some, Hypeninae, solely live off of tears (Holloway et al. 2013) whereas others, Calpinae, have barbed proboscis to pierce the flesh of mammals and feed on blood (Zenker et al. 2011). Despite extensive speciation of Lepidoptera in the tropics, there are also predators always present, awaiting a tasty meal. To avoid being eaten and survive to another day these insects employ several different antipredator tactics. They use chemical defenses, mimic toxic species, camouflage, mimic other insects, and acoustic defenses. These defenses can be costly but are necessary to survival in the tropics, a beautiful yet dangerous place.

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What better way to avoid being eaten than to taste awful? Several families of Lepidoptera use chemical defenses to be unpalatable and avoid predation. These substances can be sequestered as larva, procured from host plants, or due to de novo biosynthesis. The number of chemicals involved in these defenses are as diverse as the families which use them. Some of the chemicals which have presently been identified are: aristolochic acids, cardenolides, cyanogenic glycosides, glucosinolates, glycosidase inhibitors, iridoid glycosides, pyrrolizidine and tropane alkaloids, and pyrazines (Trigo 2000). Many of these butterflies and moths use aposematic coloration to advertise that they carry chemical defenses. Some also have urticating hairs which further irritate predators causing an intense burning sensation lasting hours. Other moths and butterflies will mimic these toxic families with similar colors and patterns but will not actually produce the chemical defense. Instead they rely upon predators learning from the toxic species to stay away.

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Aposematic coloration warns predators of toxic chemicals and urticating hairs

Crypsis, the ability to avoid observation from predators, has been mastered by Lepidoptera. Where some animals may use colors and patterns to blend into their surroundings, some of these moths take camouflage a step further by disrupt the outline of their body to become inconspicuous. Some take form of a dead leaf or a twig while others mimic lichens. This mimicry of natural objects is called mimesis. Many species within the family Geometridea and subfamily Arctiinae (e.g. lichen moths) use this tactic.

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The same subfamily Arctiinae also includes moths which mimic wasps. These moths completely change their morphology to create the illusion that they are stinging wasps. Even their movement patterns match those of the insects they are mimicking. At first glance one could easily be mistaken but by looking closely at their antenna, the moth’s true identity is revealed.

Arctiinae is an extremely diverse subfamily of moths which included 11,000 species worldwide. One of the most distinctive features of Arctiinae is their ability to use thoracic tympanal organs to detect ultrasonic calls from bats (Waters 2003) and to produce their own ultrasonic sounds with a specialized tymbal organ on their metathorax (Barber and Kawahara 2013). The males produce the sound as scales on their genital valve are moved dorsally and ventrally and grated against the inner margin of the last abdominal tergum. The females’ ultrasound production is also genitally based but has a different mechanism (Barber and Kawahara 2013). The function of these ultrasonic clicks are to jam bat sonar, startle naïve bats, and warn of unpalatability (Barber and Conner 2007).

Being a moth or butterfly in the tropics can be difficult but a number of tactics can be implemented to increase survival and fitness. Some insects use one of these strategies while others use a full arsenal. To begin to see the immense moth biodiversity that exists around you, you can hang a plain white sheet outside at night with a light shining on it. Soon the sheet will be crawling with life, mostly moths but some butterflies, beetles, and katydids as well. Each insect tells its own story of strife and success.

References

Barber JR, Conner WE. 2007. Acoustic mimicry in a predator-prey interaction. PNAS 104(22): 9331-9334.

Barber JR, Kawahara AY. 2013. Hawkmoths produce anti-bat ultrasound. Biology Letters 9(4): 20130161.

Gaston KJ. 2000. Global patterns in biodiversity. Nature 405: 220-227.

Holloway JD, Barlow HS, Loong HK, Khen CV. 2013. Sweet or savoury? Adult feeding preference of Lepidoptera attracted to banana and prawn baits in the oriental tropics. The Raffles Bulletin of Zoology 29: 71-90.

Trigo JR. 2000. The chemistry of antipredator defense by secondary compounds in neotropical lepidoptera: facts, perspectives and caveats. Journal of the Brazilian Chemical Society 11(6): 551-561.

Waters DA. 2003. Bats and moths: what is there left to learn? Physiological Entomology 28: 237-250.

Zenker MM, Penz C, De Paris M, Specht A. 2011. Proboscis morphology and its relationship to feeding habits in noctuid moths. Journal of Insect Science 11(1): 42

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Aww Snap!

Floating in the ocean, dependent on the currents to carry them, millions of zooplankton begin their life. Although invisible to the human eye, under a microscope a magical world is revealed. Over 7000 species of zooplankton fill our oceans and serve an essential role in marine food webs (Perrier et al. 2015). Some zooplankton remain small throughout development but others grow and transform into fishes, crabs, lobsters, and other animals we are familiar with. The larval forms can be unrecognizable from the mature form.

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A snapshot of marine zooplankton diversity.

Several species undergo multiple stages of development as zooplankton before reaching adulthood. Crabs are a wonderful example of this strategy. The number of planktonic larval states depends on the species of crab. These planktonic stages, known as zoea, have an appearance that resembles a shrimp unicorn hybrid. The settling state, known as megalopa, looks more like a distorted microscopic crab.

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Crab development: A) zoea and B) megalopa stages. All photographs credited to Dr. Richard R. Kib

Many species of plankton need to find a habitat in which to settle so they may grow or they will not survive. Collectively, the sessile animals which settle onto a substrate are known as epifauna. This group includes sponges, tunicates, bivalves, echinoderms, bryozoans, etc. Alexandra Hiller of Harilaos Lessios’ lab and Carmen Santiago of Mark Torchin’s lab at the Naos Marine Lab are studying recruitment of these communities. To understand how long it takes for settling to occur and the succession of this system, artificial media are introduced and monitored regularly. The two primary media are baskets filled with rocks and construction fencing, covered in mesh, and settlement plates. Both are suspended from docks and trees into the ocean. In just a couple weeks some juvenile species can be found amongst the bright orange plastic but waiting a month provides a treasure trove of magnificent organisms.

At first glance porcelain crabs pour from the baskets, scurrying every which direction. After carefully corralling of the crabs, to prevent autotomy (dropping of limbs), brittle stars emerge with delicate, spined arms.

Hard, yet squishy, clear plastic like blobs with visible digestive tracts are identified as juvenile tunicates. Tube worms create an extensive network of intertwined calcified tubules which cover the rocks. When those rocks are removed from the water, the tube worms crawl out of their homes in search of refuge. Closed anemones appear as fleshy cushions out of the water but after returning to the sea water, they slowly open to reveal their tentacles. Small, flat, undulating organisms with eye spots are identified as flat worms, but not the parasitic kind. Special care is given to centipede like fireworms whose bristlelike hairs (setae) cause intense pain, rash, redness, and swelling on contact lasting several days. The compound that causes this inflammatory response is called complanine (Nakamura et al. 2008).

The most flamboyant clade found in the baskets are nudibranchs. Not only do these gastropods come in a rainbow of colors with clashing patterns and textures, some can actually produce their own light through bioluminescence making them glow in the dark (Vallès and Gosliner 2006). Although they have a shell as larva (Page 1995) they lose it as an adult because they are so awesome they don’t need one anymore. What looks like boas one either side of their foot or tiny horns are called cerata. The cerata not only aid in respiration and gas exchange, they also protect the nudibranchs. Some nudibranchs will eat cnidarians (e.g. anemones), to steal their nematocysts (stinging cells). The nudibranch then stores the nematocysts in the tips of the cerata so to use for their own defense (Greenwood and Mariscal 1984). If that wasn’t badass enough, those cute “ears”, called rhinophores, are used for distant chemoreception and rheoreception (detection of water currents) and for contact chemoreception and mechanoreception they use their oral tentacles (Cummins et al. 2009).

As awesome as nudibranchs are, there was another animal in the baskets which tends to get more attention, the snapping shrimp. These shrimp belong to the family Alpheidae. There are about 600 species of snapping shrimp in 46 genera. These shrimp, also known as “pistol shrimp”, form symbiotic relationships with several different groups of animals (e.g. sponges, cnidarians, mollusks, echinoderms, echiurans, other crustaceans, and gobiid fishes) (Silliman et al. 2003). A rather friendly clade indeed. However, these little guys pack quite a punch. With one snap of their large claw, these shrimp have asymmetric claws, a sound is produced loud enough to be heard a kilometer away. If several alpheidae are snapping at once, it can interfere with submarine sonar (Anker et al. 2006). The sound is produced when the shrimp closes its claw so fast it alters the pressure of the surrounding water, imploding a pocket of air known as a cavitation bubble. The water jet from a snap can be received by other snapping shrimp and used to communicate or to stun prey (Versluis et al. 2000).

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Diversity of snapping “pistol” shrimp. Photograph by Steve Childs.

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Symbiotic relationship between goby and snapping shrimp. Photograph by Dennis Liberson.

Despite decades of marine research, we are barely grasping a fraction of what goes on in the waters that cover 3/4ths of the Earth’s surface. In some aspects, we know more about space than we do about what happens in the depths of our oceans. Our oceans are teeming with life, waiting to be discovered and filled with questions as well as opportunities. So next time you are going for a swim in the ocean or maybe a snorkel, remember that you are in a soup of baby animals so tiny they are invisible to the human eye. Or maybe listen to the crackling of the water, that’s the snapping shrimp communicating, hunting, or both. Whatever you do, remember you are never alone.

References

Anker A, Ahyong ST, Noël, Palmer AR. 2006. Morphological phylogeny of alpheid shrimps: parallel preadaptation and the origin of a key morphological innovation, the snapping claw. Evolution 60(12): 2507-2528.

Cummins SF, Erpenbeck D, Zou Z, Claudianos C, Moroz LL, Nagle GT, Degnan BM. Candidate chemoreceptor subfamilies differentially expressed in the chemosensory organs of the mollusk Aplysia. BMC Biology 7:28

Greenwood PG, Mariscal RN. The utilization of cnidarian nematocysts by aeolid nudibranchs: nematocyst maintenance and release in Spurilla. Tissue Cell 16(5): 719-730.

Nakamura K, Tachikawa Y, Kitamura M, Ohno O, Suganuma M, Uemura D. 2008. Complanine, an inflammation-inducing substance isolated from the marine fireworm Eurythoe complanata. Organic & Biomolecular Chemistry 6: 2058-2060.

Page LR. Similarities in form and developmental sequence for three larval shell muscles in nudibranch gastropods. Acta Zoologica 76(3): 177-191.

Perrier V, Williams M, Siveter DJ. 2015. The fossil record and palaeoenvironmental significance of marine arthropod zooplankton. Earth-Science Reviews 146: 146-162.

Silliman BR, Layman CA, Altieri AH. 2003. Symbiosis between an alpheid shrimp and a xanthoid crab in salt marshes of mid-atlantic states, U.S.A. Journal of Crustacean Biology 23(4): 876-879.

Vallès Y, Gosliner TM. 2006. Shedding light onto the genera (Mollusca: Nudibranchia) Kaloplocamus and Plocamopherus with description of new species belonging to these unique bioluminescent dorids. The Veliger 48(3): 178-205.

Versuluis M, Schmitz B, von der Heydt A, Lohse D. 2000. How snapping shrimp snap: through cavitating bubbles. Science 289(5487): 2114-2117.

Not just another Newton

Flowers release chemical cues to attract pollinators, some smell pleasant to humans while others smell like feces or rotting flesh, the chemical signature is designed for each plants’ ideal pollinator. But what happens when the flower is inside of the fruiting body? The answer is complex but we are starting to understand.

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Our story starts with the delicious and nutritious fruiting bodies of the ficus genus, figs. Unlike some other plants which attract bats, birds, bees, flies, butterflies or moths to pollinate their flowers, figs depend on wasps only a few millimeters long. You see, the flowers of figs are inside the unripe fruit and only these tiny wasps can crawl inside the ostiole (small opening) of the fruit. Without fig wasps, figs would not survive. Figs and fig wasps have evolved together for 70-90 million years. There are around 850 species of figs and each has at least one dominate pollinator (wasp species). Frequently there will be two species or an entire list of wasp species that pollinate a single species of fig. These wasps have mostly been identified morphologically, leading scientists to believe that we only described a small portion of the existing species.

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Diversity of pollinators: hummingbirds, sweat bees (copyright Clay Bolt/claybolt.com), bumblebees (copyright Clay Bolt), and bats.

The female wasp who enters the fig is known as the foundress. The foundress will enter the fig and crawl to a cluster of flowers inside known as the inflorescence. There she will pollinate some of the female flowers and lay her eggs, both male and female, before she dies. Galls form where the eggs are deposited. Male wasps emerge from the galls first. The only job of the males is to fertilize their sisters who are trapped inside galls and chew a hole to let the females escape. Then the males will die, never leaving the fig, but the females emerge fertilized and gather pollen before finding a new unripe fig to deposit their eggs. Their life outside the fig sometimes only lasts a day. Sounds bizarre, right? Well fig wasps aren’t the only insects with such behavior. Many species of Heliconius butterflies exhibit pupal mating strategies.

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Male Heliconius butterfly mating with a female pupa. Notice an adult female has deposited two eggs on the female pupa’s head.

All figs on a particular tree will ripen at the same time so that when the female fig wasps emerge they are forced to go to another tree. How does a tiny wasp find another fig tree of the same species with unripe fruit over a long distance? Well scientists believe that they use olfactory signals and chemostimulation (Gibernau & Hossaert-McKey 1998). Finding another tree doesn’t ensure oviposition, in fact some females must fight to the death to crawl into a fig to pollinate it, deposit eggs, and die. Aggressive species will even decapitate competitors (Dunn et al. 2015).

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Gas chromatography showed that receptive fig extract is composed of ten compounds. The principal chemical compounds, making up over 75%, are linalool, linalool oxide, and benzylalcohol (Gibernau & Hossaert-McKey 1998).

The relationship described here is a mutualism between figs and fig wasps but nature is known to be filled with cheats and fig wasps are no exception. What happens if a foundress decides not to pollinate the fig in which she deposits her eggs? Frequently fig trees will abort any fruit that has not been pollinated and this will kill the wasp’s eggs in it, punishing the cheaters.

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Mutual relationship between figs and fig wasps on the left. Cheating situation on the right where the female fig wasp never pollinates the fig, only deposits her eggs.

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Adult female fig wasps emerging from a fig.

So, the question becomes, are you eating helpless baby wasps when you grab a fig newton? The answer is no. Most commercial fig production comes from dioecious trees meaning there are two sexes. The male fig tree will produce fruit which will have the wasp galls and when the wasps hatch they will pollinate the fruits of both the female and male trees but will only deposit their eggs in the fruit of the male tree. Thus, leaving those figs of the female tree with only seeds inside. Some people call the figs of the male tree goat figs because people will purchase a bag of the figs from a male ficus and hang it in their female tree to make use of the wasps but then they collect only the fruit from the female tree and feed the left-over goat figs to…well their goats. Goats have such an extensive history of eating figs that some fig wasp species have changed their oviposition site due to goat predation (Zamora & Gómez 1993). Some commercial varieties of figs are sterile, like seedless watermelons or bananas, and do not require pollination. Other ficus trees are monoecious meaning the tree will have both male and female flowers on the same tree. These figs will have the seeds and wasp galls. If you ate the figs of these trees, you might end up with a dissolved foundress, the dead males or some wasp larva but figs produce an enzyme (ficain) which digests any dead wasps and use those nutrients to grow so it is unlikely you’ll find any presents. Knowing all this, will it affect your consumption of figs? Hopefully it just makes you appreciate this supple fruit even more and its little wasp friends. If it still grosses you out, then fig get about it.

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References

Dunn DW, Jandér KC, Lamas AG, Pereira RAS. 2015. Mortal combat and competition for oviposition sites in female pollinating fig wasps. Behavioral Ecology 26(1): 262-268.

Gibernau M, Hossaert-McKey M, Frey J, Kjellberg F. 1998. Are olfactory signals sufficient to attract fig pollinators? Ecoscience 5(3): 306-311.

Zamora R, Gómez JM. 1993. Vertebrate herbivores as predators of insect herbivores: an asymmetrical interaction mediated by size difference. Oikos 66: 223-228.

Lessons from the 50-hectare plot

In the middle of the Panama Canal lays a 1,500-hectare island created by mankind during the formation of the canal. This island once was a mountain top but when its valleys flooded, all the animals on the mountain were faced with new challenges. Ten years after becoming an island in 1923, the United States Government deemed Barro Colorado Island (BCI) a nature reserve. It was one of the earliest of its kind in the Americas. An entomologist from Chicago, Dr. James Zetek, was appointed director of the small field station called Canal Zone Biological Area (CZBA) which later evolved into a world-renowned facility now known as the Smithsonian Tropical Research Institute. Researchers from around the world took advantage of the unusual set of circumstances that created BCI and started studying the biodiversity of the island as well as changes in such over time.

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BCI is an ideal location to test principles of island biogeography theory, such as colonization and extinction rates and long term effects of isolation on species richness and abundance. In the past decade, there has been a strong focus on the decline of plant and animal species on BCI and the underlying causes. Robinson (2001) reported a ≥50% decline in 37 species of birds on BCI in 25 years and Karr (1982) reported 50-60 species of birds disappeared from BCI since its separation from the mainland. Meanwhile Stapley et al. (2015) examined 40 years of data on tropical lizards on BCI and found a population decline correlating with the southern oscillation index of the previous year, suggesting that rainfall and temperature are driving factors of population fluctuation. Basset et al. (2015) hypothesized that plant-animal interactions were the cause of local extinctions (6%) and population declines in butterfly species (decrease of 211 species in 90 years) but many species disappeared without the loss of their host plant, bringing us back to the question of why.

Looking back at the ideas of Wilson and MacArthur, if there is decreased colonization then events such as drought, floods, etc. could bring the decline or extinction of a species on an island. Since the plants and animals on BCI had evolved to be mountain species where they are separated from other populations mostly by elevation, the lake surrounding the mountain (Gatun Lake) changed the dynamics and species flow. Moore et al. (2008) designed an experiment to look at the dispersal limitations of understory bird populations by capturing 10 different common understory specialists and releasing them from a boat at multiple distances (100, 200, and 300 meters) from BCI to see how far these birds could fly before crashing into the lake of exhaustion. Note: birds that failed to make it to the island were recovered, dried off, and returned to the site of capture. The long-billed hermit (Phaethornis longirostris), a hummingbird, was the only bird able to fly 300 meters back to BCI. The Checker-throated Antwren (Myrmotherula fulviventris) failed to make it even 100 meters. These birds would not need to fly far in the understory and have evolved under conditions of dense forest. While living on a mountain they could make their way to new regions through the forest but since 1913 these birds have been trapped, unable to leave the island.

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One of the most impressive features of BCI, from the scientific perspective, is the dedication of a 50-hectare plot of tropical forest in 1980. In the plot, every plant ≥1 cm in diameter has been numbered and is censused every 5 years. No manipulative research is allowed in the area, only observational so one study will not negatively impact another. This accompanied with climatic environmental data and arthropod abundance helps not just plant biologists, but also ornithologists, primatologists, herpetologists, etc. Several researchers have found El Niño events to cause fruit shortages on BCI leading to the famine of many different species (e.g. deer, peccaries, coatis, agoutis, howler monkeys, and capuchin monkeys) (Foster 1982, Wright et al. 1999, Milton et al. 2005). From December 2010 to February 2011 Milton and Giacalone (2013) found BCI capuchin monkey populations decreased 72-77% while the howler monkey population remained relatively stable. Typically, capuchin monkeys heavily rely upon arthropods in December because few ripe fruits are available. Milton and Giacalone hypothesized that the negative impacts of heavy rainfall on arthropod populations led to the great number of capuchin deaths. Howler monkey populations were believed to not be negatively impacted because during this time they primarily consume young leaves. This is a great example of how the multitude of research efforts being conducted at BCI can amalgamate.

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On the way to the 50-hectare plot seed traps begin to pop up around the base of trees, a little closer and neon flagging tape sets one tree apart from its brethren. Stepping into the plot, passing an invisible line, the forest is covered in aluminum tree tags, flagging tape everywhere, as far as the eye can see. Some trees have data loggers on them, metal bracelets hold equipment to the trunk with foil insulation covers, others have PVC pipe coming out of them. A living, outdoor laboratory.

On our journey, we had several researchers telling us of their own projects being conducted in the 50-hectare plot. They each knew every individual plant they worked with and formed a true connection with their study species. After hiking across the entire island to find a specific Zanthoxylum ekmanii tree that one of the researchers had been working with for 5 years, we found that tropical storm Otto had knocked it down as well as several other trees on that side of the island. We were all deeply saddened by the loss of this great tree but took comfort in knowing that even in death it would provide life to other organisms in the forest. Now, its thousands of seeds will be provided an opening in the canopy to obtain light, which is vastly limited in the rainforest, and perhaps one will take the place of its maternal source.

References

Basset Y, Barrios H, Segar S, Srygley RB, Aiello A, Warren AD, Delgado F, Coronado J, Lezcano J, Arizala S, Rivera M, Perez F, Bobadilla R, Lopez Y, Ramirez JA. 2015. The butterflies of Barro Colorado Island, Panama: local extinction since the 1930s. PLOS One 10(8): 1-22.

Foster RB. 1982. Famine on Barro Colorado Island. In: Leigh EG, Rand AS, Windsor DM, editors. The ecology of a tropical forest. Washington, DC: Smithsonian Press. p 201–212.

Karr JR. 1982. Avian extinction on Barro Colorado Island, Panama: a reassessment. The American Naturalist 119(2): 220-239.

Milton K, Giacalone J. 2013. Differential effects of unusual climatic stress on Capuchin (Cebus capucinus) and Howler monkey (Alouatta palliata) populations on Barro Colorado Island, Panama. American Journal of Primatology 76(3): 1-13.

Milton K, Giacalone J, Wright SJ, Stockmayer G. 2005. Do frugivore population fluctuations reflect fruit production? Evidence from Panama. In: Dew L, Boubli JP, editors. Tropical fruits and frugivores: the search for strong interactors. Dordrecht, the Netherlands: Springer. p 5–36.

Moore RP, Robinson WD, Lovette IJ, Robinson TR. 2008. Experimental evidence for extreme dispersal limitation in tropical forest birds. Ecology Letters 11: 960-968

Robinson WD. 2001. Changes in abundance of birds in a Neotropical forest fragment over 25 years: a review. Animal Biodiversity and Conservation 24(2): 51-65

Stapley J, Garcia M, Andrews RM. 2015. Long-term data reveal a population decline of the tropical lizard Anolis apletophallus, and a negative affect of El Nino years on population growth rate. PLOS One 10(2): 1-14

Wright SJ, Carrasco C, Calderon O, Paton S. 1999. The El Nino southern oscillation, variable fruit production and famine in a tropical forest. Ecology 80: 1632–1647.