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Reproductive strategy of a cave-living arachnid with indeterminate growth (Phrynus longipes; Amblypygi: Phrynidae).

Natural selection predicts that organisms should maximize reproductive fitness by optimizing the tradeoff between the quantity and quality of offspring (Lack 1947, 1954; Smith & Fretwell 1974). This was intuitively posited because organisms have limited resources available in the environment with which to produce offspring. Thus, increasing the quantity of offspring decreases the investment available for each offspring. This tradeoff between quantity and quality has resulted in different reproductive strategies, e.g., r- and K-selection (Pianka 1970). Here, we test for a tradeoff between offspring quality and quantity in the amblypygid Phrynus longipes (Pocock, 1894).

Species of the order Amblypygi (Arachnida) have a unique combination of life history traits that provide no clear intuition about the likelihood of exhibiting a tradeoff. Unlike nearly all other arthropods, amblypygids have indeterminate growth and continue to molt after sexual maturity (Weygoldt 2000; Chapin & Hebets 2016). Thus, unlike most other arthropods, amblypygid initial egg size is unlikely to determine final adult size (Smith 1997). Many arthropods with indeterminate growth produce higher quality offspring as they age (Fox & Czesak 2000). For example, older female water fleas (order: Cladocera) with indeterminant growth produce eggs that are larger than the optimal size (Bell 1983; Boersma 1997). Amblypygids are long-lived (perhaps 7-10 years), iteroparous, and produce 10-90 eggs per clutch (Fig. 1; Chapin & Hebets 2016). Amblypygids exhibit high parental care relative to arthropods that typically exhibit a quantity-quality tradeoff (Chapin & Hebets 2016). Females carry the eggsac on the ventral opisthosoma (Fig. 1a). After hatching, young emerge and climb onto the back of the female where they molt before becoming free-living (Figs. 1b,c; Weygoldt 2000; Chapin & Hebets 2016). Thus, amblypygids provide postembryonic parental investment that may limit clutch size and obscure the quantity-quality tradeoff (Boyce & Perrins 1987; Oksanen et al. 2001; Gilbert & Manica 2010; but see Walker et al. 2008). Evolutionary history also provides no clear hypothesis for a tradeoff occurring in P. longipes; the closely related Araneae tend to not show the tradeoff, but scorpions do (Killebrew & Ford 1985; Marshall & Gittleman 1994; Brown 2003; Skow & Jakob 2003), and the phenomenon is common among other arthropod groups (Berrigan 1991; Fox & Czesak 2000).

The tradeoff is often detected in semelparous species that exhibit low parental care and use larval-acquired resources to produce eggs (Ford & Seigel 1989; Fox & Czesak 2000). However, the tradeoff is often not detected in taxa with iteroparity and parental care as these factors complicate life history and obscure existing tradeoffs (Gilbert & Manica 2010). In addition, the quantity-quality tradeoff is more obvious in oviparous species, which, unlike viviparous species, allocate a discrete amount of resources to offspring upon or soon after fertilization (Ford & Seigel 1989; King 1993). Egg-laying animals provide finite resources to developing young, which should emphasize energetic constraints on offspring number and quality (Parker & Begon 1986). Spider egg mass scales geometrically with egg diameter and spider eggs have constant energy density (Anderson 1990). We assume the same is true for whip spiders, such that larger eggs require greater energy investment, but often have higher survivability. Larger eggs experience lower rates of desiccation (Anderson 1990; Sota & Mogi 1992). In addition, progeny that arise from larger eggs have better feeding performance (Walker et al. 2003) and may be less resistant to starvation (Gliwicz & Guisande 1992; Wallin et al. 1992). Thus, we tested whether the amblypygid, Phrynus longipes, exhibits a tradeoff between the quality and quantity of offspring, with the goal of expanding our understanding of variation in parental investment across arthropods.

We collected twenty-four egg-carrying Phrynus longipes from Cueva Matos (ca. 18.38[degrees]N, 66.68[degrees]), Arecibo, Puerto Rico in August 2014. We measured the maximum prosoma width of each female using digital calipers to the nearest 0.1 mm [+ or -] 0.1 mm. The prosoma shows allometric growth throughout the life of amblypygids and correlates well with body mass (Chapin 2011; Chapin & Hebets 2016). We stored specimens in 95% ethanol and shipped them to our laboratory at UCLA for further analysis. We recorded the total number of eggs per female and dry mass of eggs from each clutch. We placed individual eggs in microcentrifuge tubes and dried them in a drying oven at 60[degrees]C for 120 h. We weighed dried eggs with a microbalance scale to the nearest 1 [micro]g [+ or -] [micro]g (Orion Cahn C-33). Further, we determined the developmental stage of each egg, and if the embryo was developing.

We compared generalized linear models (GLM) of egg mass predicting egg count with female size as a covariate using Akaike's information criterion corrected for small sample size (AICc) and Akaike's weights (wi; Burnham et al. 2011; Symonds & Mousalli 2011). We used post hoc linear regressions to examine the relationship between mean egg mass, total egg count, and female size separately.

Phrynus longipes had a clutch size of 67 [+ or -] 3.3 eggs (x [+ or -] s; range: 29-94; n = 24 clutches). Overall, eggs mass was 4.01 [+ or -] 0.12 mg (Range: 3.10-5.21 mg) and the prosoma width of females was 15.80 [+ or -] 0.36 mm (range: 12.3-18.9 mm). The best GLM predicting egg count included only female size, not mass (Table 1; estimate [+ or -] s = 5.806 [+ or -] 1.473, [t.sub.23] = 3.940, P < 0.001). Larger females (measured as prosoma width) laid more eggs per clutch (adjusted [r.sup.2] = 0.435, [F.sub.1, 21] = 17.96, P < 0.001; Fig. 2a) but female prosoma width failed to predict egg mass (adjusted [r.sup.2] = 0.012, [F.sub.1, 21] = 1.268, P = 0.273; Fig. 2b). Egg developmental stage or the proportion of embryos that developed did not improve model results.

We did not detect a quality-quantity tradeoff in P. longipes (Fig. 2). Larger females had a higher number of eggs but not lower quality offspring, measured as egg mass. Larger females invest more resources into producing more eggs rather than investing more into each egg. Our results support the findings of Fox and Czesak (2000): species that do not show a quantity-quality tradeoff are often iteroparous, use adult-acquired resources for reproduction, or provide postembryonic parental care, all of which are characteristics of P. longipes (Fox & Czesak 2000).

Our results generally align with patterns seen in Araneae with few differences that can be attributed to life-history (Killebrew & Ford 1985; Marshall & Gittleman 1994; Brown et al. 2003; Skow & Jakob 2003; Barrantes 2015). Larger, and therefore older, P. longipes females laid larger clutches. This is the opposite pattern seen in many arthropods, including Araneae, which lay smaller successive clutches with age (Marshall & Gittleman 1994; Fox & Czesak 2000; Brown et al. 2003). Female Araneae generally lay only a few clutches in their lifetime while female amblypygids can generally produce one to three clutches a year over their lifetime of perhaps as many as 10 years (Weygoldt 2000; Chapin & Hebets 2016). Clutches are expected to become smaller with age in arthropods that acquire resources as larva and deplete reserves with age (Wasserman & Asami 1985; Boggs 1986; Fox 1993) or where short or variable lifespans make future reproduction uncertain. Phrynus longipes, however, has a long lifespan and survivorship probabilities likely increase with age.

Amblypygids exhibit indeterminate growth and continue to molt after maturity. Many arthropods with indeterminate growth produce higher quality offspring as they age (Bell 1983; Boersma 1997; Fox & Czesak 2000;). Surprisingly, older, larger female P. longipes produce more but not larger eggs. Amblypygi eggs might already be of an optimal size, such that provisioning resources to eggs might not benefit offspring. Instead, amblypygids invest in a great number of offspring.

Our cave study site provides exceptionally high levels of prey, so we assumed there would be low variation in resource acquisition (Chapin 2015; Chapin & Hill-Lindsay 2016). This is important, because variation in resource acquisition can obscure a tradeoff between size and quantity (van Noordwijk & de Jong 1986). For example, resource scarcity results in unequal rates of resource acquisition and investment in clutches among female conspecifics which may conceal an existing tradeoff (van Noordwijk & de Jong 1986). Intraspecific experiments indicated a tradeoff under high, but not low, resources abundance (Brown 2003). Variable resource acquisition, however, can mask these effects. Despite this, no tradeoff was detected in P. longipes between egg size and quantity. Although females are unlikely to be limited by resource acquisition, other factors could potentially prevent a tradeoff from being detected.

Future research should quantify how egg mass impacts survivorship and reproductive fitness. For example, egg size may be influenced by physiological constraints on eggs, including oxygen absorption, nutritional accessibility, and desiccation. Further investigation into factors influencing egg size in amblypygids will provide insight into the diversity of parental investment in arthropods and reveal the unique life history of amblypygids.

ACKNOWLEDGMENTS

This research was funded by a Student Research Grant from the Animal Behavior Society, the American Philosophical Society's Lewis and Clark Fund for Exploration and Research, the Explorers Club Exploration Fund, the UCLA Latin American Institute via a donation from the Faucett Catalyst Fund, the UCLA's Edwin W. Pauley Fellowship, and the Department of Ecology and Evolutionary Biology Fellowship. Thanks to Peter Nonacs and the Nonacs Lab for advice and feedback. Thanks also to field assistants Alma Basco, Laura Caicedo, Patrick Casto, Kimberly Dolphin, Jose Sanchez, Chelsea Vretenar, and Daniel E. Winkler. Research was conducted under the Puerto Rico Department of Natural Resources and the Environment permit number 2012-IC-064.

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Kenneth James Chapin and Emily Katherine Chen: Department of Ecology & Evolutionary Biology, University of California, Los Angeles, 612 Charles E. Young Drive East, Los Angeles, CA 90095-7246; E-mail: chapinkj@gmail.com.

Manuscript received 8 August 2017, revised 26 January 2018.
Table 1.--Multimodel comparisons of generalized linear models
predicting egg count (n = 24) in clutches of Phrynus longipes. The full
model includes egg mass, female size, and their interaction as
predictor variables. Female size, but not mass, best predicted egg
count.

Model           AICc    k  [DELTA]AICc  [w.sub.i]

mass x size     199.12  4   0.00          0.06
mass + size     196.22  3  -2.90          0.26
size            194.33  2  -4.80          0.67
mass            204.93  2   5.81        < 0.001
intercept only  204.76  1   5.63        < 0.001
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Title Annotation:SHORT COMMUNICATION
Author:Chapin, Kenneth James; Chen, Emily Katherine
Publication:The Journal of Arachnology
Article Type:Report
Date:May 1, 2018
Words:2582
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