vol. 175, no. 2

the american naturalist



february 2010

Notes and Comments Is Diet Quality an Overlooked Mechanism for Bergmann’s Rule? Chuan-Kai Ho,1,* Steven C. Pennings,1 and Thomas H. Carefoot2 1. Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204; 2. Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada Submitted February 20, 2009; Accepted August 21, 2009; Electronically published December 16, 2009 Online enhancement: appendix.

abstract: Bergmann’s rule (body size increases with latitude) has long interested biologists; however, its mechanism remains unclear. An overlooked mechanism (latitudinal variation in plant quality) might help explain Bergmann’s rule. We studied three herbivores. In the field, the planthopper Prokelisia and the sea hare Aplysia, but not the long-horned grasshopper Orchelimum, were larger at high latitudes, following Bergmann’s rule. In the laboratory, all three species grew larger or faster on high-latitude plants. High-latitude diets increased Prokelisia size and Aplysia growth rates by 8% and 72%, respectively, enough to explain the increase in field body size toward high latitudes. Therefore, latitudinal variation in herbivore body size could be influenced by latitudinal variation in plant quality, which may directly or indirectly also affect body size in detritivores, parasitoids, and predators. Studies of Bergmann’s rule should consider the influence of biotic factors on body size in addition to abiotic factors such as temperature and precipitation. Keywords: body size, herbivore, plant quality, latitudinal variation, biogeography, Spartina alterniflora.

Introduction Biologists are interested in how abiotic and biotic factors generate ecological patterns, not just because we wish to understand how organisms are shaped by their environment but also because we seek to predict what will happen given future environmental changes. One of the most striking ecological patterns that has been discovered is Bergmann’s rule, which states that body size tends to increase with latitude or with lower temperatures (Bergmann 1847; Mayr 1956). Bergmann’s rule was originally proposed for endotherms and is obeyed by 76% of birds and 71% of mammals (Millien et al. 2006). Surprisingly, however, Bergmann’s rule is also obeyed by about 80% of ectotherms (Atkinson 1994; Walters and Hassall 2006). * Corresponding author. Present address: Department of Marine Biology, Texas A&M University, Galveston, Texas 77551; e-mail: [email protected]. Am. Nat. 2010. Vol. 175, pp. 269–276. 䉷 2009 by The University of Chicago. 0003-0147/2010/17502-51095$15.00. All rights reserved. DOI: 10.1086/649583

Body size has profound effects on the physiology and life history of an organism, as well as an organism’s interactions with other individuals or species (Werner et al. 1983; Partridge and French 1996; Brown et al. 2004). Since Bergmann’s rule states that body size varies across geographic regions, it has drawn the attention of both ecologists and evolutionary biologists (Blanckenhorn and Demont 2004; Blanckenhorn et al. 2006; Stillwell et al. 2008). However, despite over a century of study, the mechanisms underlying Bergmann’s rule are still unclear. It was originally proposed that temperature explained Bergmann’s rule in endotherms (Bergmann 1847; Mayr 1956). Under this scenario, larger animals are favored at low temperatures because their lower surface area-to-volume ratio creates an advantage in conserving body heat. This explanation for Bergmann’s rule has largely been discounted for endotherms (Ashton et al. 2000; Freckleton et al. 2003) and is even less compelling for ectotherms, especially those that are small or aquatic, whose body temperature largely fluctuates with ambient temperature. An alternative explanation for Bergmann’s rule came from the perspective of life history (Atkinson 1994; Partridge and French 1996; Angilletta et al. 2004). Basically, this explanation suggested that organisms are selected to delay maturation in colder environments and therefore reach a larger adult size despite a slower growth rate. While temperature and other abiotic factors that covary with latitude, such as rainfall, have been the primary focus of efforts to understand Bergmann’s rule (James 1970; Sand et al. 1995; Azevedo et al. 1996; Van Voorhies 1996; Ashton et al. 2000; Millien et al. 2006; Walters and Hassall 2006; Yom-Tov and Geffen 2006), biotic factors that vary with latitude (e.g., food availability) have only occasionally been examined (McNab 1971; Arnett and Gotelli 2003). To our knowledge, the role of food quality in explaining Bergmann’s rule has not been directly examined, although past authors have speculated that food quality may vary with latitude and consequently affect animal body size (e.g., Langvatn and Albon 1986; Herfindal et al. 2006).

270 The American Naturalist Plant quality (e.g., chemical defenses, nitrogen content) often varies across latitude, with better plant quality at high latitude (Bolser and Hay 1996; Siska et al. 2002; Wright et al. 2004; C.-K. Ho and S. C. Pennings, unpublished manuscript). Given that plant quality is likely critical to herbivore growth, it is reasonable to speculate that better plant quality at high latitudes might support better growth of herbivores, leading to Bergmann’s rule. Although this explanation is limited to herbivores, they represent a substantial proportion of animal species. Moreover, similar mechanisms might operate at other trophic levels if larger herbivores represent a better resource for higher trophic levels (see “Discussion”). In summary, we argue that the focus on seeking abiotic explanations for Bergmann’s rule has caused biologists to overlook biotic factors that might contribute to latitudinal patterns in body size. Here, we examine the hypothesis that food quality contributes to latitudinal patterns in body size of three herbivore species. We tested two predictions: (1) in the field, herbivores will be larger at high latitudes, consistent with Bergmann’s rule, and (2) in the laboratory, plants collected from high latitudes will support better growth of herbivores, suggesting that variation in plant quality across latitude could contribute to Bergmann’s rule. Methods Study Species We studied three herbivore species: the planthopper Prokelisia marginata, the long-horned grasshopper Orchelimum fidicinium, and the sea hare Aplysia juliana. All species will be referred to generically hereafter. The inclusion of two terrestrial herbivores and one marine herbivore ensured that our results were not habitat specific. Prokelisia, a multivoltine planthopper, is the most abundant herbivore species in low salt marshes in the Atlantic and Gulf Coasts of the United States (Denno et al. 1985, 1996). Prokelisia is a phloem-feeding specialist on Spartina alterniflora, which is one of the most abundant plants in salt marshes along the Atlantic and Gulf Coasts of the United States. On the Atlantic Coast of North America, the distribution of Spartina ranges from Florida to Quebec (USDA 2009). Orchelimum, a univoltine long-horned grasshopper, is one of the most abundant orthoptera found on S. alterniflora in the Atlantic Coast of the United States; it extends from Florida into New England but is rare north of Virginia (Wason and Pennings 2008). Orchelimum feeds heavily on S. alterniflora and, like many tettigoniids, also includes arthropod prey in its diet (Smalley 1960; Pennings et al. 2001). Aplysia is an opisthobranch gastropod with a cosmopolitan distribution, occurring over a wide range of

latitude, from New Zealand through northern Japan (Eales 1960; Carefoot 1987). Aplysia consumes green algae of the genus Ulva throughout most of its range (Carefoot 1987) and also consumes the brown alga Undaria pinnatifida in temperate waters (Saito and Nakamura 1961).

Patterns of Body-Size Variation in the Field To document patterns in body size across latitude for these three herbivore species, we collected new data from fieldcollected specimens or referred to published data. From July 16 to 28, 2007, we used sweep nets to collect hundreds of Prokelisia individuals from Spartina plants located along creek banks at each of 15 salt marsh sites (table A1 in the online edition of the American Naturalist) from Florida to Massachusetts, over 12⬚ of northern latitude. We randomly selected 20 adults/site and measured their body length from the frons (tip of the head) to the end of the abdomen. We calculated the average body length for males and females separately for each site, examined the effect of sex on body size using an ANCOVA with latitude as a covariate, and evaluated the interactive effect between latitude and sex on body size by comparing the regression slope between sexes. We obtained body-size data for Orchelimum from Wason and Pennings (2008). They measured tibia length as an indicator of body size of adult Orchelimum that were collected from 20 salt marsh sites from Florida to Rhode Island, over 11⬚ of northern latitude, from 2004 to 2006 (19 individuals/site, on average). We calculated the average tibia length for males and females separately for each site and analyzed the data the same way as for Prokelisia. Tibia length was a less variable measurement than body length for Orchelimum because animals adopted a variety of more or less “hunched” postures after collection; nevertheless, analyses of body length and tibia length led to identical conclusions. Since Aplysia has a flexible body and indeterminate growth, we used maximum body mass as the best indicator of variation in body size. We extracted data on maximum body size of Aplysia from published studies conducted in the Southern (Tanzania, Brazil, Australia, New Zealand) and Northern (Barbados, Hawaii, Florida, Okinawa, Japan) Hemispheres (see fig. 1 legend). In addition, data from six locations were added using our unpublished observations and personal communications from other scientists. The final data set covered over 35⬚ of latitude in each hemisphere. Since Aplysia is a simultaneous hermaphrodite, we did not divide the data by sex.

Diet Quality and Bergmann’s Rule 271 Do Diets from Different Latitudes Affect Herbivore Performance in the Laboratory? To examine how host plants from different latitudes affect the performance of herbivores, we conducted factorial growth experiments (plant origin # herbivore origin) with Prokelisia and Orchelimum and a single-factor (plant species) experiment with Aplysia. To simplify the design of experiments with Prokelisia and Orchelimum, we grouped the sites from which we collected plants and herbivores into high-, medium-, and low-latitude regions (5 sites/ region; table A1). The Prokelisia experiment was a 3 (plant regions) # 3 (Prokelisia regions) factorial design, with five replicates of each combination of regions. We collected Spartina plants (N p 5/site) and Prokelisia adults from May 30 to June 11, 2006, at the same sites described above (table A1). Spartina were potted in a mixture of 60% potting soil and 40% sand; no fertilizer was added. Prokelisia (N p 20/site) were cultured in polyester cages on additional Spartina plants collected from their native sites. Prokelisia and Spartina were brought to the greenhouse on Sapelo Island, Georgia. Once these Prokelisia produced offspring in August 2006, three juveniles (fourth instar, two stages before adulthood) from each site were reared on caged Spartina. Twice a week, we removed individuals that had reached adulthood, and we measured their body length. We scored Prokelisia for sex when they were adults because it is difficult to determine the sex of juveniles. Data were analyzed as a three-way ANOVA, with plant region, herbivore region, and sex as main effects. We did not measure initial size of Prokelisia because we wished to minimize handling of delicate nymphs; therefore, we analyzed final adult size rather than growth rate. The Orchelimum experiment was a 3 (plant regions) # 2 (Orchelimum regions) factorial design because Orchelimum was too rare to collect successfully at the highlatitude sites. Each combination of regions had an average of eight replicates (N p 15 for each plant region; N p 22, 23 for Orchelimum from medium- and low-latitude regions). We collected Spartina plants (N p 8/site) from May 30 to June 11, 2006, at the same sites described above and potted them in a mixture of 60% potting soil and 40% sand; no fertilizer was added. Because Orchelimum has only one generation a year (Smalley 1960), we used field-collected individuals instead of laboratory-raised juveniles for the laboratory experiment. Orchelimum juveniles (fourth instar, two stages before adulthood) were collected from July 16 to 28, 2006, from the same field sites described above (except the high-latitude region). On July 29, 2006, we measured the body mass and tibia length of each Orchelimum and placed each individual into a glass jar with a Spartina leaf freshly cut from a plant from a

high-, medium-, or low-latitude site. Leaves were replaced every 2 days. After 1 month, we remeasured body mass and tibia length. Since adult Orchelimum become prevalent in the field about 2 months after the peak of nymph abundance (C.-K. Ho and S. C. Pennings, personal observations), a 1-month laboratory experiment represents a large proportion of the growth period of Orchelimum. Data analysis was similar to that in the Prokelisia experiment. We quantified the impact of plant diet on Orchelimum individuals by calculating their relative growth rate in size, (ln S 1 ⫺ ln S 0 )/DT, since not all of them reached adulthood or survived the same period of time; S1, S0, and DT represent final size, initial size, and time period, respectively. The Aplysia experiment reflected the natural distribution of its host plants across latitude. We conducted experiments with Aplysia at the Noto Marine Laboratory (37⬚30⬘N, 137⬚10⬘E), Noto Peninsula, Japan, in 1993. Rocky intertidal and shallow subtidal areas near the laboratory are dominated by the algae Ulva and Undaria. Aplysia (32–116-g initial mass) were collected near the laboratory, blotted dry with a towel, weighed, maintained in the laboratory on a diet of Ulva (a low-latitude diet), Undaria (a high-latitude diet), or both (N p 9, 8, and 9, respectively) with food replaced daily, and reweighed after 7 days. Aplysia performance was quantified as relative growth rate in body mass, (ln M1 ⫺ ln M 0 )/DT, since Aplysia has a flexible body, a relatively long (16 months) postmetamorphic life span, and indeterminate growth; M1 and M0 represent the body mass in the end and at the beginning of the experiment, respectively. Results Patterns of Body-Size Variation in the Field Two out of three species followed Bergmann’s rule, while one species showed the opposite pattern. Prokelisia were larger at higher latitudes, and females were larger than males (no latitude # sex interaction; fig. 1A). In contrast, Orchelimum were smaller at higher latitudes, with females again larger than males (no latitude # sex interaction; fig. 1B). Aplysia were an order of magnitude larger at high than at low latitudes, but the relationship was stepwise rather than linear (fig. 1C). Aplysia were typically less than 50 g in mass at most low-latitude sites but commonly reached over 500 g at high-latitude sites in Japan and New Zealand. Do Diets from Different Latitudes Affect Herbivore Performance in the Laboratory? In all three species, diet significantly affected herbivore performance. Prokelisia grew larger when fed plants from

272 The American Naturalist high- versus low-latitude regions (fig. 2A). As in the field, females were larger than males (fig. 2A), and there was no interaction between plant region and sex (P p .74; table A2 in the online edition of the American Naturalist). Orchelimum grew faster when fed plants from high- versus low-latitude regions (fig. 2B). In this case, sex neither affected growth rate (fig. 2B) nor interacted with plant region (P p .70; table A2). Aplysia grew faster when fed Undaria, a major component of its diet at high latitudes, than when fed Ulva, its diet at low latitudes (fig. 2C; table A2). A mixture of both Undaria and Ulva was not superior to Undaria alone. Herbivore region did not affect Prokelisia body length or Orchelimum tibia growth rate (P p .11 and .91, respectively) but did interact with sex in the Orchelimum experiment (P p .04; table A2). We did not address herbivore region for Aplysia because we studied animals only from one geographic region. Discussion

Figure 1: Latitudinal variation in body size of Prokelisia (A), Orchelimum (B; data from Wason and Pennings 2008), and Aplysia (C). For Aplysia, numbers in parentheses indicate the number of independent observations at each location: New Zealand (Willan and Morton 1984), Australia (P. D. Steinberg, personal communication), Brazil (Marcus and Marcus 1955 and Marcus 1958 combined to make one data point), Tanzania (Bebbington 1974), Barbados (Carefoot 1980), Hawaii (Edmundson 1946; Sarver 1978; Kay 1979; Switzer-Dunlap and Hadfield 1979; T. H. Carefoot, personal observations), Florida (Pilsbry 1951), Okinawa (T. H. Carefoot, personal observations; S. C. Pennings, personal observations), Japan (Saito and Nakamura 1961; Usuki 1970; S. C. Pennings and T. H. Carefoot, personal observations for two locations).

All three species grew faster or attained larger sizes when fed foods representing a high- versus a low-latitude diet. This supports our hypothesis that variation in plant quality across latitude could contribute to explaining Bergmann’s rule. The two species that follow Bergmann’s rule in the field, Prokelisia and Aplysia, represent a dioecious, terrestrial species and a hermaphroditic, marine species, respectively. The fact that both show the same pattern reveals the potential for plant quality to explain body-size patterns in herbivores representing different ecological systems and life-history traits. Because plant quality is known to change across latitude in both marine and terrestrial systems (Bolser and Hay 1996; Siska et al. 2002; Wright et al. 2004; Toju and Sota 2006; C.-K. Ho and S. C. Pennings, unpublished manuscript), latitudinal variation in plant quality could help explain Bergmann’s rule in a wide variety of herbivores. Both phenotypic plasticity and heritable differences in body size are likely to contribute to Bergmann’s rule. For example, studies on how environmental factors affect body size, that is, the temperature-size rule (Atkinson 1996), tend to explain Bergmann’s rule on the basis of phenotypic plasticity (Angilletta and Dunham 2003). In contrast, studies of Drosophila have tended to focus on genetically based variation in body size among populations (Partridge and French 1996; Huey et al. 2000). Our field data could reflect the result of both plasticity (to food quality) and heritable difference in body size since these two factors are confounded in the field. Our laboratory data, however, should solely reflect plasticity in body size since the experimental design controlled for herbivore origin. While this study was not intended to untangle the relative importance of

Diet Quality and Bergmann’s Rule 273

Figure 2: A–C, Effect of diet on laboratory growth of Prokelisia (A), Orchelimum (B), and Aplysia (C). D, Body length of Prokelisia raised in the laboratory on host plants from three latitudinal regions (X-axis) versus the body length of individuals collected in the field from three latitudinal regions (Y-axis). Dotted line indicates a 1 : 1 relationship. Data are means ⫹ 1 SE.

plasticity and genetic control, these two factors could be related via genetic assimilation or accommodation (WestEberhard 2005; Braendle and Flatt 2006) and deserve further investigation. For Prokelisia, animals raised in the laboratory were smaller than animals collected in the field (fig. 2D), likely reflecting the fact that animals in the laboratory were not able to move among plants and select the most nutritious ones on which to feed. The variation in body size among Prokelisia raised on host plants from different latitudes (about an 8% increase from low- to high-latitude diets) was similar to the variation observed in the field (about a 5% increase from low to high latitudes). This suggests that plant quality alone could explain Bergmann’s rule in Prokelisia. Similarly, Prokelisia raised on plants from a single latitude grew 10% larger on fertilized than on control

plants (Cook and Denno 1994), again suggesting that variation in plant quality alone could explain the magnitude of variation in body size observed across latitude. Spartina plants from high latitudes are higher in quality likely because they are softer and have a higher nitrogen content and reduced chemical defenses compared with plants from low latitudes (Siska et al. 2002; C.-K. Ho and S. C. Pennings, unpublished manuscript). These differences in plant quality were constitutive, rather than induced by the environment (Salgado and Pennings 2005). For Aplysia, a high-latitude diet including Undaria increased growth rate by 55% (Undaria alone) to 72% (Undaria and Ulva) compared to a low-latitude diet of Ulva. Such a difference in growth rate, compounded over several weeks, would easily lead to the order-of-magnitude difference in body mass observed in the field. In the case of

274 The American Naturalist Aplysia, there is also evidence that latitudinal variation in temperature could play a role in body size. Aplysia grown through their entire postmetamorphic life at 20⬚C were twice as big as those at 28⬚C (roughly, summer water temperatures of central Japan and Hawaii, respectively; Hadfield and Switzer-Dunlap 1990). However, water temperature alone is unlikely to be the primary factor determining body size since water temperature varies continuously with latitude, but the observed latitudinal pattern of maximum body mass in Aplysia is discontinuous—a step function (fig. 1C). This step function is, however, consistent with the pattern that might be produced by an abrupt shift to a new diet driven by the distributional limit of Undaria. In addition, the magnitude of variation produced by laboratory temperature experiments (twofold; Hadfield and Switzer-Dunlap 1990) was too small to explain the variation in the field (tenfold). We conclude, therefore, that latitudinal variation in diet could be a large part of the explanation for Bergmann’s rule in Aplysia. For Orchelimum, laboratory results were similar to those obtained with Prokelisia and Aplysia: a diet of high-latitude plants led to faster growth than a diet of low-latitude plants. In the field, however, Orchelimum showed the converse to Bergmann’s rule, which is observed less often than Bergmann’s rule (Atkinson 1994; Millien et al. 2006). This suggests that factors other than plant quality (or temperature) were more important in determining latitudinal variation in Orchelimum body size in the field. An explanation for the converse to Bergmann’s rule is that the shorter growing season at high latitudes selects for fast developmental time and, hence, smaller body size (Mousseau 1997). Support for this hypothesis comes from the fact that Orchelimum is largely replaced at high latitudes by a related long-horned grasshopper Conocephalus spartinae that is about 33% smaller (Wason and Pennings 2008). Growing-season length might represent less of a constraint for Prokelisia, which is multivoltine (Denno et al. 2003), or for Aplysia, which grows throughout the entire year (S. C. Pennings and T. H. Carefoot, personal observations). Since some salt marsh arthropods are more abundant at low than at high latitudes (Pennings et al. 2009), another possible explanation for the converse to Bergmann’s rule in field Orchelimum is that Orchelimum might eat a diet with a higher proportion of animal prey at low latitudes, leading to better growth. So far, our argument that latitudinal variation in plant quality could help explain Bergmann’s rule applies only to herbivores, but this argument could be extended to cover other types of consumers. For example, high-quality litter derived from high-quality plants might support better growth of detritivores at high latitudes (Greenwood et al. 2007, for a local example). Because parasitoids can attain larger sizes in larger hosts (Kouame´ and Mackauer

1991), latitudinal variation in herbivore body size might also drive latitudinal variation in parasitoid body size. Similarly, larger herbivores at high latitudes might support larger body sizes in predators. Even if these speculations are not borne out in future studies, herbivores represent a large proportion of animals, and so our results may represent an important, if partial, mechanism contributing to Bergmann’s rule. In this note, we have emphasized the importance of diet in contributing to Bergmann’s rule because this mechanism has been largely overlooked (but see Stillwell et al. 2007). We do not intend to dismiss the importance of abiotic factors (e.g., temperature, rainfall) in also contributing to latitudinal variation in body size. Rather, we would suggest that, in many cases, Bergmann’s rule may be best explained by some combination of biotic and abiotic factors, rather than any single, universal explanation. In particular, a large number of laboratory studies have shown that variation in temperature can affect body size (Anderson 1973; Partridge et al. 1994; Atkinson 1996). As mentioned above, temperature probably plays a role in latitudinal variation in Aplysia body size but by itself cannot explain the shape or the magnitude of the body-size variation. In addition, biotic factors (such as food quality) might interact with abiotic factors to drive the pattern of body size. For example, life-history theory suggests that colder environments (i.e., high latitude) favor organisms with delayed maturation and bigger adult size. In the field, better food quality at high latitudes might enable organisms to tolerate a harsh environment and delay maturation. Furthermore, if biotic interactions (i.e., predator-prey interactions) vary across latitude, then higher predation pressure might select for larger prey because of size refuges from predation (Werner et al. 1983; Bro¨nmark and Miner 1992) or smaller prey because of early maturation (Wilbur and Fauth 1990). Therefore, we encourage future studies of Bergmann’s rule to expand beyond a focus on abiotic factors to consider diet and other biotic factors that might interact with abiotic factors to produce latitudinal variation in body size. Acknowledgments We thank the National Oceanic and Atmospheric Administration’s National Estuarine Research Reserve (NERR) Graduate Research Fellowship (GRF) program (NA04 NOS 4200137), National Science Foundation (OCE9982133, DEB-0296160, 0638796, 0709923), and Natural Sciences and Engineering Research Council of Canada for funding and the Ashepoo, Combahee, and Edisto Basin Reserve for serving as the GRF host reserve. We thank staff from 12 NERR and three Long-Term Ecological Research (LTER) sites, especially L. Blum, T. Buck, C. Buzzelli, M.

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