Author Spotlight: The Need for New Categorizations of Dietary Specialism in Animals

13 09 2016

Emilio Pagani-Núñez, Craig A. Barnett, Hao Gu & Eben Goodale

Guangxi University, Nanning, Guangxi Zhuang Autonomous Region, People’s Republic of China

 

Moreover, it is not understood when a species will evolve a particular niche width through the device of being polymorphic with phenotypes which are resource specialists, monomorphic with one generalist phenotype, or some intermediate condition.                                                 J. Rouhgarden (1974) The American Naturalist, 108 (962): 429-442

 

Certain ideas are rapidly and broadly accepted by the scientific community, sometimes even by a whole society.  This is the case of the concepts of ‘generalism’ and ‘specialism’, which have improved our understanding of ecological and evolutionary processes in nature.  However, to some extent, many authors have stressed the need to review and reformulate the existing theory about diet specialization.  This motivated us to write our review article “The need for new categorizations of dietary specialism incorporating spatio-temporal variability of individual diet specialization”, published in the September 2016 issue of the Journal of Zoology.

jzo-september-2016-cover-image_jzo-11-15-r-362r1_cropped

Great tit nestling (Parus major), photo by Emilio Pagani-Nunez

At present, there is no consensus among researchers on a definition of diet specialization. We searched papers defining great and blue tits as ‘generalists’ or ‘specialists’ and we observed a great inconsistency among authors in how they classified the two species.  Traditionally, diet specialization was conceptualized as a continuous gradient from totally generalist species to completely specialized species that were behaviourally and physically adapted to eat specific food types. However, the discovery of individual diet specialization (IDS) challenges the traditional gradient of specialization within and among species. IDS means that, within species and populations, different individuals can specialize in the exploitation of different subsets of the available resources.

Species with broad diets and widespread distributions can provide useful examples of how species theoretically considered as generalists can show a surprising level of specialization at both the population and the individual level. Conversely, irrespective of distribution range, species inhabiting variable environments can evolve strikingly variable levels of specialization among individuals from both spatial and temporal perspective. In this paper, we reviewed the literature on specialization in great tits and blue tits.  Both species are considered caterpillar specialists at the centre of their ranges, but this reliance on caterpillars declines at the periphery of their ranges (e.g. the Mediterranean).  Specifically, we found that great tits show a higher level of IDS than blue tits do, developing new dietary specializations when the most common prey is not available.

Another issue that has not been well explored in the literature is the role of foraging innovations in promoting novel dietary specializations. Research in foraging innovations also has a long history of research (e.g. the opening of milk bottle tops by great and blue tits in United Kingdom). There have been few attempts to link foraging innovations to the capacity to evolve contrasting levels of specialization from the species to the individual level. However, the capacity for foraging innovations may explain why certain ‘generalist’ species show such contrasting levels of specialization between populations and individuals.

Here, we introduce a new categorization of specialization that takes into account all these factors.  We define obligate specialists as species composed of individuals that are primarily adapted to exploiting a single resource (e.g. hummingbirds). Facultative specialists are species in which individuals are adapted to exploit a single food type or niche, but occasionally they can exploit alternative food resources (e.g. birds of prey). Facultative generalists are species composed of individuals that are able to develop novel specializations to preferably exploit alternative resources, (e.g. great tits and sea otters).  Finally, obligate generalists are able to exploit a wide variety of resources (or one if it is very abundant), with a limited capacity to incorporate foraging innovations (e.g. many passerine species).

By publishing our new classification, our aim is to provide clearer and more workable definitions of diet specialization within and among populations and species. We also are interested in initiating a debate among ecologists about the necessity of incorporating IDS as well as spatial and temporal variation into studies of foraging ecology.  This general framework is also attractive because it is applicable to a wide variety of taxa and makes comparison among taxa easier.

 





New Journal of Zoology Podcast

10 08 2016

A new episode of the Journal of Zoology podcast is now available and you can listen to it here.

JZO_butterfly_podcast_imageIn this episode, Tim Thurman and Brett Seymoure talk to us about their study on two mimetic butterflies and how similar they appear to the eyes of their predators, we will learn from Lucy Lush how biologging technology can improve our ability to record and analyse wild animal behaviour, and we are told by Niklas Björklund how ants can help protect conifer seedlings from pests in forest plantations via non-consumptive interactions with pine weevils.

You may subscribe to iTunes to receive the latest Journal of Zoology podcasts.





Winner of the 2015 Journal of Zoology ‘Paper of the Year’ award

2 08 2016

JoZ Blog

Biochemical correlates of aggressive behavior in the Siamese fighting fish

M. D. Regan, R. S. Dhillon, D. P. L. Toews, B. Speers-Roesch, M. A. Sackville, S. Pinto, J. S. Bystriansky and G. R. Scott

 

Aggressive interactions between individuals of the same species can result in the evolution of exaggerated body traits that improve success in these interactions, and subsequently, access to resources such as food and mates. Although conspicuous morphological adaptations such as antlers are usually what come to mind, metabolic processes that occur hidden within cells are required to sustain aggressive behaviour, so their enhancement may also be important for a successful outcome.

Siamese fighting fish, Betta splendens Siamese fighting fish, Betta splendens; photo by Dave Toews

With this in mind, we designed a study to examine the intersection of aggressive behaviour and metabolic biochemistry using the Siamese fighting fish, a staple of the world’s pet shops. Male Siamese fighting fish are notoriously…

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21st Century Lizards: Small, Rare and Trendy – Author Spotlight with Shai Meiri

18 07 2016

 

When I was a kid, what passed for phylogenetic trees in the illustrated books I used to read, were drawings showing not just the relationships (often vaguely drawn) between groups, but also their diversity. In such drawings mammals were invariably shown (correctly!) as having increased hugely in diversity after the KT. Reptiles on the other hand, were shown to be in decline after the Mesozoic, and the lines depicting diversity of lizards and snakes were invariably very thin, much more so than those depicting mammals and birds. As an undergraduate student (late) in the previous millennium I was taught that there are a lot of birds, and many mammals, but that amphibians and reptiles are relatively minor groups, with fewer species than in either endotherm class. Ten years ago, when I started studying lizards (i.e., resumed what I used to do as a kid, chasing lizards around, but nowadays calling it a profession) I knew this wasn’t the case. But had I known just how many lizard species are going to be recognized nowadays, I might have despaired and never started. Simply put – reptile taxonomists are running rampant, discovering, splitting, and describing about 200 new species every year: the number of recognized lizard species has increased by 31% since the turn of the century. As a macroecologist I try desperately to keep up.

Photo 1 Cyrtodactylus durio by Lee Grismer

Cyrtodactylus durio, described in Malaysia in 2010 by Grismer et al. Photo by Lee Grismer

Who are all these new lizards, which the writers of children’s nature books and the professors who taught me zoology never knew? And why were they described only recently? In a study now published in Journal of Zoology I set out to check.

My first thoughts were to blame eroding species concepts (“taxonomic inflation”), certainly a major cause of elevating subspecies to species level, as well as to recognize new species that older generations of taxonomists would have ranked as mere varieties, or ecotypes within polytypic species. Alternatively, new species may be difficult to detect because they inhabit places that previous generations of herpetologists seldom visited, and have restricted ranges. Likewise, they may have individual-level traits making them difficult to detect: perhaps they are small? Or are active at night? Or below ground (or high in the canopy)?

Some of those hypotheses were already examined in other animal taxa. Using my macroecological database of lizard traits, and data on the distribution of all reptiles we are now finishing to assemble (see http://www.gardinitiative.org/index.html), I now explicitly tested them for the 1323 lizard species described in the 21st century until the beginning of my study (just under a year ago, the number is already 1406 as of April 2016).

Photo 2 graph from the paper

The locations where lizards have been described during the 21st century (dots). Warmer colours signify more descriptions in that country.

If species splitting was the cause, then I would not necessarily reveal many changes in the traits of “new” (i.e., described this century) and “old” species (those described between 1758 and 1999). But I did identify some interesting differences: as is usually the case, newly described species have small distribution ranges. They are also more likely than old species to be threatened with extinction and suffer population declines. New lizards are also small bodied, and often nocturnal (geckos are especially dominant). It seems that the greatest increase in species description rates has occurred in Southeast Asia. This century, new species of lizards have been described in 96 countries, mostly Australia (105 species), Argentina (103), Vietnam (66), Brazil (64), Madagascar (60), Malaysia (58), and the Philippines (48). Africa, however, saw relatively few new descriptions – I assume this reflects geopolitical reasons rather than postulate that we have anywhere near complete lists of African lizards. Similarly, relatively few burrowing species have been described this century – and I think this is likely to reflect our ignorance, rather than a comprehensive knowledge of burrowing forms such as amphisbaenians and dibamids. These assumptions are nearly testable (one can certainly refute them…).

Photo 3 Cnemaspis psychedelica by Lee Grismer

The aptly named Cnemaspis psychedelica, described on an island off the shore of Vietnam in 2010 by Grismer et al. Photo by Lee Grismer

When and at what number of species will this stop? How many species of lizards exist and when will we know them all? Unfortunately, given the accelerating rates of species descriptions, these are questions I cannot answer.

But the species that are being discovered are far from boring, dull, or ugly – some are strikingly beautiful. We need to keep on cataloging them, caring about them, and protecting them.

Shai Meiri

Tel Aviv University

 





Author Spotlight: The Astonishing Bites of Crocodilians and How They Do It

15 06 2016

Ontogenetic bite-force modeling of Alligator mississippiensis: implications for dietary transitions in a large-bodied vertebrate and the evolution of crocodylian feeding

P. M. Gignac and G. M. Erickson

Alligators and crocodiles are impressive predators that can generate up to 3,000 and 4,000-pound bite forces, which they use to subdue large prey such as deer and wildebeests. To put that much force into perspective, being captured in the jaws of a large crocodilian is comparable to being pinned beneath a 2016 Ford Mustang, or having Dwayne “The Rock” Johnson stand on you with another dozen Dwayne “The Rock” Johnsons standing on him. You may have heard before that these animals are the living kings of chomp, brandishing the title for the most forceful bites measured in any animal to date. Not only is that true, but today’s species are not even the largest crocodilians to have ever lived—not by far.

So, how is it even possible for an animal to generate this much force?

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Paul Gignac holding the head of a 12-foot American alligator during a bite force test. Photo by Joern Hurum

That is a super question, and it is the central focus of our new study. Our research team has been working with these animals for more than a decade, trying to understand their unique lifestyles and how they make a living. Before this research we measured the bites of every living crocodilian species, and we were astonished to discover how much force is behind them. In our new Journal of Zoology study we dissected a growth series of American alligators to examine how the jaw musculature changes across development. We documented muscle position, arrangement, and—particularly—fascicle orientations, which allowed us to build mathematical models of theoretical bite forces that incorporated muscle morphology, position, physiology, and activation. We tested these models against the bite forces we had measured directly (in vivo) for similarly sized animals, and our calculations turned out not to differ from the in vivo values.

We then went back into the experimentally validated models and looked at how muscle positions, sizes, and force outputs changed from hatchlings through large-bodied adults. We found that all muscles had meaningful contributions to those 3,000 and 4,000-pound bite forces, but one muscle in particular called the “ventral pterygoideus” was the major player. If you have ever seen a crocodilian for yourself, you might have thought that it had oddly thick neck. Well, it turns out, that is not all neck! The ventral pterygoideus muscle is so large that it spill out behind the head and wraps around the jaw, attaching from below and behind. This muscle makes up about half of the overall muscle mass that goes into generating a bite, but it contributes more than 60% of the bite force in most individuals and an astonishing 70% in exceptionally large adults.

This one muscle is so large that it could not fit inside the head, where the other jaw muscles are housed, even if it was the only one. Instead, it seems that over time this muscle was pushed backwards towards the animal’s neck, which allowed it to become massive while also maintaining the fairly low-profile skull that is typical of crocodilians. As a result, these near-shore predators can hide in shallow water to ambush animals that come too close for a drink, while also being capable of sustaining the thousands of pounds of bite force necessary to capture and consume such prey.

We also discovered a few particulars about this large muscle that are important. For instance, it has fascicles arranged in a chevron pattern (like a “V”), similar to those in your calf muscles or deltoids, which is a great way to pack a lot of force into a given volume of space. So not only is the ventral pterygoideus muscle enormous, but it is also particularly good at generating force, even for its large size.

It is this combination of traits that have helped crocodilians become masters of their domain since the age of the dinosaurs. Our next step is to figure out how they got to be this way by plotting out the evolution of the crocodilian jaw system across 240 million years of its evolutionary history from a gracile and svelte morphology to the intimidating and powerful one we commonly think of today.





Author Spotlight: How long do giant squid grow?

1 06 2016

Unleashing the Kraken: on the maximum length in giant squid (Architeuthis sp.)

C.G.M. Paxton, University of St Andrews

Anecdotal accounts of giant squid length are longer than actual measured specimens. And scientists’ estimates of maximum giant squid length are shorter than actual measured specimens. The reason for this seeming paradox is that the longer measurements are thought to be inaccurate, or the result of stretching of the tentacles (the two longest arms). A new study by Dr Charles Paxton of the University of St Andrews suggests that, given the variation in length exhibited in measured specimens, giant squid of total length of 20 m are rather probable, although some of the giants reported as anecdotes may be exaggerations or inaccuracies.

jzo12347-toc-0001-m

Architeuthis clarkei. Plate I in Robson (1933), vol. 103, issue 3, Proceedings of the Zoological Society of London

The length of the longest specimen of giant squid ostensibly measured is 19 m (extracted from the gut of a sperm whale from the Indian Ocean) but the roundness of the figure is suspicious, and the 19-m figure is not wholly reconcilable with the photo that accompanies it. Another specimen of 16.81 m length was described in New Zealand in 1888, however the ratio of the two long tentacles to the mantle (body) length was suspiciously high, leading some researchers to suggest that the tentacles were stretched.

Nevertheless, if the spread of the lengths in available specimens is considered and, given the length of the longest reliably measured mantle (the squid’s “body”) known, 2.79 m, squid of total length of a least 20 m are not implausible. There remains the interesting question of the maximum length of squid that could be taken by the only known predator of adult giant squid, the sperm whale? From the indigestible beaks of the squid found in the guts of sperm whales, a minimum estimate can be made, and it appears that adult bull sperm whales have swallowed giant squid with mantle length of at least 2.69 m. Given that it is unlikely that we have found the longest specimen of giant squid ever eaten by a sperm whale, it remains plausible that large bull sperm whales could take squid as much as 3 m in mantle length, a fight that would be the most awesome wildlife scene yet to be captured on camera.

Charles Paxton

 





Author Spotlight: Sexual dimorphism in the horned isopod

12 05 2016

Sexual dimorphism and physiological correlates of horn length in a South African isopod crustacean

D.S. Glazier, S. Clusella-Trullas and J.S. Terblanche

 

Figure 1

Dr. Susana Clusella-Trullas on the left and Dr. John Terblanche in the middle along the rocky shore where specimens of the horned isopod (Deto echinata) were collected. Photo by Douglas Glazier

During October 2012 to March 2013 I spent a wonderful sabbatical leave at Stellenbosch University in South Africa.  There I was hosted by two superb physiological ecologists, Drs. John Terblanche and Susana Clusella-Trullas, who also happen to be husband and wife.  My major objective was to compare the rates of metabolism and water loss of several species of amphipod and isopod crustaceans with differing degrees of adaptation to land life. During one of my field trips to Pringle Bay (Western Cape Province) along the southern coast of South Africa, John and Susana acquainted me with the unusual horned isopod (Deto echinata) that lives abundantly amongst piles of wave-washed rocks along the shore (see Fig. 1).   I was immediately fascinated by the extremely long dorsal spines of the males of this species (Fig. 2), which I had never seen before in any other isopod species that I had collected in many places around the world.

Figure 2

A male horned isopod. Photo by Douglas Glazier

Most isopod species that dwell along rocky shores are notoriously difficult to capture – their association with sea shores and their quick escape responses to intruders has led to them to be called “sea roaches”.  However, I soon learned a useful technique for capturing dozens of these animals in a matter of seconds!  All I had to do was to reach my hand into one of the wet rock crevices (Fig. 3) and legions of these creepy crawlers would quickly scurry up my arm and beyond, reminding me of the scary scarab beetle attack scene in the 1999 movie “The Mummy”.   All I had to do next was to shake or brush my arm over a collection bucket and my collection was complete!

Figure 3

Example of a rocky crevice where I collected numerous individuals of the horned isopod. Photo by Douglas Glazier

Back at John Terblanche’s laboratory I soon realized that the dorsal spines of D. echinata are not only longer in males than females, but they increase disproportionately in length as a male grows in size.  In fact, the scaling slope of male horn length in relation to body length is one of the steepest ever observed for a morphological trait.  My guess was that this extreme “positive allometry” of a sexually dimorphic trait was likely due to sexual selection.  My working hypothesis was that male horn length is a sign of “health”, “strength” or genetic fitness that could influence female mate choice.  An important aspect of fitness is the successful ability to acquire, conserve and store resources.  With the help of John and Susana, I tested this hypothesis by measuring the body condition (body mass per length), activity levels, and rates of energy use and water loss of male D. echinata with different horn lengths (Figs. 4, 5).

Figure 4a

Figure 4b

Examples of male Deto echinata with relatively short and long dorsal spines. Photo by Douglas Glazier

Figure 5

Dr. Terblanche’s laboratory at Stellenbosch University where the rates of metabolism and water loss were measured in individual males of the horned isopod. Photo by Douglas Glazier

As expected, males with relatively long horns had significantly better body condition and faster rates of resting metabolism than males with shorter horns.  However, activity level and rate of water loss were not related to horn length.  It thus seems possible that male horn length is a reliable signal of “good genes” to potential female mates or rival males, thus favoring its evolutionary increase via sexual selection.   Direct observations of female mate choice and male-male competition for mates are needed to further test this hypothesis.

Douglas Glazier